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ADAM KUSPA

TitleSenior Vice President and Dean of Research
InstitutionBaylor College of Medicine
DepartmentOffice of the President
AddressONE BAYLOR PLAZA
HOUSTON TX 770303498
Email
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    Other Positions
    TitleProfessor
    InstitutionBaylor College of Medicine
    DepartmentDepartment of Biochemistry & Molecular Biology
    DivisionBiochemistry & Molecular Biology

    TitleProfessor
    InstitutionBaylor College of Medicine
    DepartmentDepartment of Molecular & Human Genetics
    DivisionMolecular & Human Genetics

    TitleProfessor
    InstitutionBaylor College of Medicine
    DepartmentDepartment of Pharmacology
    DivisionPharmacology


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    Collapse Biography 
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    1995 - 1997Searle Scholar, Knship Foundation
    1995 - 1998ACS Junior Faculty Research Award, American Cancer Society
    2005Elected Fellow AAAS, American Association for the Advancement of Science
    2005Michael E. DeBakey Excellence in Research Award, Baylor College of Medicine
    2011Michael E. DeBakey Excellence in Research Award, Baylor College of Medicine

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    Summary
    Dr. Kuspa’s research involves the use of Dictyostelium to study problems of development and host-pathogen interactions, with an emphasis on cellular communication, cell differentiation and innate immunity. Dr. Kuspa initiated genomic studies in Dictyostelium as a postdoctoral fellow – a project that led to a collaboration with Dr. Richard Gibbs and the Human Genome Sequencing Center at BCM and culminated in the completion of the first amoebal genome sequence in 2005. With Dr. Gad Shaulsky at BCM, Dr. Kuspa also pioneered the functional analysis of the genome by developing methods for gene function discovery. Dr. Kuspa’s laboratory has also discovered novel determinants of Legionella pathogenesis involving the cleavage of Dictyostelium’s mitochondrial ribosomal rRNA and conserved proteins involved in vesicular trafficking. Recently, Dr. Kuspa's laboratory discovered an innate immune system in Dictyostelium mediated by TIR domain signaling pathways. Intriguingly, mutants in this pathway are defective in immune function during development and are compromised in their bacterial feeding behavior during vegetative growth. The apparent requirement of innate immune functions for growth on bacteria suggests that innate immunity evolved from bacterial foraging mechanisms in the progenitor of the crown group eukaryotes.

    Development in a simple system
    A long-term goal of Dr Kuspa’s is to define the cellular regulatory mechanisms that govern cell differentiation in eukaryotes using Dictyostelium as a model. This system can be used to provide a complete picture of the regulation of a significant biological problem: the integration of individual cells into distinct tissues with the proper form and function. Dictyostelium cells normally live as solitary amoebae in the soil, consuming other microbes by phagocytosis. Upon starvation, ~50,000 cells aggregate into a mound and become an integrated multicellular organism with distinct tissue types. Each organism consists of about 70% prespore cells and 30% prestalk cells. When conditions are favorable, they form a fruiting body, the terminal developmental structure that is made up of a sorus of dormant spores held aloft on a cellular stalk. The similarity between Dictyostelium and human genes provides a system where the function of protein ensembles can be tested in a simple system and the results applied to understanding the function of those proteins in other systems. Previously, we had studied two ABC transporters, RhT and TagA, that operate very early in development and which control aspects of initial cell differentiation. We have also characterized several components of the regulatory network that governs the growth to development transition itself: a novel putative receptor/kinase GdtB, a conserved protein kinase YakA and a conserved translational regulator PufA. These five regulators form critical links in the regulatory network that controls growth, the decision to initiate development.

    Genome Sequencing Project
    The Dictyostelium sequencing effort resulted in a highly accurate sequence of 34 million basepairs encoding 12,500 protein-coding genes. Amoebozoa such as Dictyostelium are noteworthy as representatives of one of the surviving branches of the crown group of eukaryotes. Comparisons between representatives of these branches (plants, amoebae, fungi and animals) promises to shed light not only on the nature and content of the ancestral eukaryotic genome, but on the diversity of ways in which its components have been adapted to meet the needs of complex organisms. The genome of Dictyostelium, as the first amoebozoa to be fully sequenced, should be particularly informative for these analyses. Accordingly, Dictyostelium has been designated by the NIH as one of the “model organisms”.

    Functional Genomics
    Functional genomics holds the promise that we can define the functions of cells and organisms by using genome-scale techniques to obtain a global view of biological systems. The Kuspa laboratory has begun large-scale functional analyses of the Dictyostelium genome, in collaboration with Gad Shaulsky and Richard Sucgang here at BCM, and Blaz Zupan at the University of Ljubljana in Solvenia. We are developing the technology that will allow us to generate and characterize mutants at a genomic scale. We have initiated a large-scale mutagenesis and “parallel phenotyping” project utilizing molecular barcodes. Recently, we have defined normal development from the viewpoint of the transcriptional profile of populations of cells using RNAseq, providing a robust “transcriptional fingerprint” of development that describes the major transitions in Dictyostelium development and defines the main cell types. This work has put us in a position to analyze mutants by comparison of their transcriptional profiles. The advantages of transcriptional profiling are now obvious since the method can be applied in a uniform way, it provides a universal phenotype and no prior knowledge of the mutated gene is required. Classical epistasis analysis can determine the order of function of genes in pathways using morphological, biochemical and other such phenotypes. It requires knowledge of the pathway’s phenotypic output and a variety of experimental expertise, so it is unsuitable for genome-scale analysis. We have demonstrated the utility of transcriptional profiles of mutants as phenotypes for epistasis analysis by determining known and unknown epistatic relationships between genes and by reconstructing genetic networks.

    Studies of bacterial pathogenesis
    We have begun a project to examine host-pathogen interactions using Legionella infection of Dictyostelium as a model. Ralph Isberg and Howard Shuman have shown that Legionella bacteria infect and kill Dictyostelium amoebae in a manner similar to the way they kill human cells. We are using the genomic approaches described above to define the host cell components required for pathogenicity. Insights gained from Dictyostelium are then applied to cell culture models of human cell infection. In one study, we found that the mitochondrial large subunit ribosomal RNA (LSU rRNA) of Dictyostelium is cleaved during Legionella infection. Mapping the cleavage sites during a time-course of infection suggests that rRNA cleavage takes place in two sequential steps. A single initial cleavage site is predicted to be on the surface of the D. discoideum mitochondrial ribosome, distinct from the site attacked by the castor bean toxin ricin. Two additional sites that appear to be cleaved later occur at the interface with the ribosome small subunit. These findings suggest that L. pneumophila infection disrupts mitochondria function in D. discoideum. Functional L. pneumophila type II and type IV secretion systems are required for the cleavage, which is the first molecular event observed to require both pathogenesis related export functions. Since the cleavage of the LSU rRNA is predicted to disrupt mitochondrial function, the requirement of these two secretion systems establishes a correlation between the pathogenesis of L. pneumophila and D. discoideum rRNA cleavage. LSU rRNA cleavage was not observed in infections of Acanthamoeba castellanii or human U937 cells, suggesting that L. pneumophila uses distinct mechanisms to interrupt the metabolism of different host cells.

    Innate immunity
    Innate immunity allows plants and animals to sense microbial pathogens and mount a defensive response. In animals this function is carried out by specialized immune cells that use cell surface toll-like receptors (TLRs) to sense the presence of pathogens and effect appropriate physiological responses. Amoebozoa diverged from the animals and fungi after the plant/animal split and are thought to have lost innate immune functions since amoebae are single-celled organisms and would have no obvious need for an immune response to pathogens. We have discovered a cell type that arises during multicellular development of Dictyostelium which appears to provide a form of innate immunity. Several homologs of innate immunity signaling genes in other organisms are expressed in these cells and a mutation in one of those, a TIR domain containing protein, causes increased susceptibility to killing by Legionella. In addition, this mutant is defective in feeding on non-pathogenic bacteria. The requirement of an innate immunity protein for growth on bacteria suggests that innate immunity evolved from bacterial foraging mechanisms in early eukaryotes.


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    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    1. Zhang X, Zhuchenko O, Kuspa A, Soldati T. Social amoebae trap and kill bacteria by casting DNA nets. Nat Commun. 2016; 7:10938. PMID: 26927887; PMCID: PMC4773522.
    2. Žitnik M, Nam EA, Dinh C, Kuspa A, Shaulsky G, Zupan B. Gene Prioritization by Compressive Data Fusion and Chaining. PLoS Comput Biol. 2015 Oct; 11(10):e1004552. PMID: 26465776.
      View in: PubMed
    3. Hirose S, Santhanam B, Katoh-Kurosawa M, Shaulsky G, Kuspa A. Allorecognition, via TgrB1 and TgrC1, mediates the transition from unicellularity to multicellularity in the social amoeba Dictyostelium discoideum. Development. 2015 Oct 15; 142(20):3561-70. PMID: 26395484.
      View in: PubMed
    4. Miranda ER, Nam EA, Kuspa A, Shaulsky G. The ABC transporter, AbcB3, mediates cAMP export in D. discoideum development. Dev Biol. 2015 Jan 15; 397(2):203-11. PMID: 25448698; PMCID: PMC4277735.
    5. Waheed A, Ludtmann MH, Pakes N, Robery S, Kuspa A, Dinh C, Baines D, Williams RS, Carew MA. Naringenin inhibits the growth of Dictyostelium and MDCK-derived cysts in a TRPP2 (polycystin-2)-dependent manner. Br J Pharmacol. 2014 May; 171(10):2659-70. PMID: 24116661; PMCID: PMC4009007.
    6. Robery S, Tyson R, Dinh C, Kuspa A, Noegel AA, Bretschneider T, Andrews PL, Williams RS. A novel human receptor involved in bitter tastant detection identified using Dictyostelium discoideum. J Cell Sci. 2013 Dec 1; 126(Pt 23):5465-76. PMID: 24006265; PMCID: PMC4376016.
    7. Miranda ER, Zhuchenko O, Toplak M, Santhanam B, Zupan B, Kuspa A, Shaulsky G. ABC transporters in Dictyostelium discoideum development. PLoS One. 2013; 8(8):e70040. PMID: 23967067; PMCID: PMC3743828.
    8. Ho HI, Hirose S, Kuspa A, Shaulsky G. Kin recognition protects cooperators against cheaters. Curr Biol. 2013 Aug 19; 23(16):1590-5. PMID: 23910661; PMCID: PMC3759992.
    9. Nasser W, Santhanam B, Miranda ER, Parikh A, Juneja K, Rot G, Dinh C, Chen R, Zupan B, Shaulsky G, Kuspa A. Bacterial discrimination by dictyostelid amoebae reveals the complexity of ancient interspecies interactions. Curr Biol. 2013 May 20; 23(10):862-72. PMID: 23664307; PMCID: PMC3914002.
    10. Santorelli LA, Kuspa A, Shaulsky G, Queller DC, Strassmann JE. A new social gene in Dictyostelium discoideum, chtB. BMC Evol Biol. 2013; 13:4. PMID: 23298336; PMCID: PMC3559258.
    11. Hirose S, Benabentos R, Ho HI, Kuspa A, Shaulsky G. Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science. 2011 Jul 22; 333(6041):467-70. PMID: 21700835; PMCID: PMC3142563.
    12. Sucgang R, Kuo A, Tian X, Salerno W, Parikh A, Feasley CL, Dalin E, Tu H, Huang E, Barry K, Lindquist E, Shapiro H, Bruce D, Schmutz J, Salamov A, Fey P, Gaudet P, Anjard C, Babu MM, Basu S, Bushmanova Y, van der Wel H, Katoh-Kurasawa M, Dinh C, Coutinho PM, Saito T, Elias M, Schaap P, Kay RR, Henrissat B, Eichinger L, Rivero F, Putnam NH, West CM, Loomis WF, Chisholm RL, Shaulsky G, Strassmann JE, Queller DC, Kuspa A, Grigoriev IV. Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biol. 2011; 12(2):R20. PMID: 21356102; PMCID: PMC3188802.
    13. Cabral M, Anjard C, Malhotra V, Loomis WF, Kuspa A. Unconventional secretion of AcbA in Dictyostelium discoideum through a vesicular intermediate. Eukaryot Cell. 2010 Jul; 9(7):1009-17. PMID: 20472692; PMCID: PMC2901666.
    14. Parikh A, Huang E, Dinh C, Zupan B, Kuspa A, Subramanian D, Shaulsky G. New components of the Dictyostelium PKA pathway revealed by Bayesian analysis of expression data. BMC Bioinformatics. 2010; 11:163. PMID: 20356373; PMCID: PMC2873529.
    15. Parikh A, Miranda ER, Katoh-Kurasawa M, Fuller D, Rot G, Zagar L, Curk T, Sucgang R, Chen R, Zupan B, Loomis WF, Kuspa A, Shaulsky G. Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol. 2010; 11(3):R35. PMID: 20236529; PMCID: PMC2864575.
    16. Khare A, Santorelli LA, Strassmann JE, Queller DC, Kuspa A, Shaulsky G. Cheater-resistance is not futile. Nature. 2009 Oct 15; 461(7266):980-2. PMID: 19794414.
      View in: PubMed
    17. Rot G, Parikh A, Curk T, Kuspa A, Shaulsky G, Zupan B. dictyExpress: a Dictyostelium discoideum gene expression database with an explorative data analysis web-based interface. BMC Bioinformatics. 2009; 10:265. PMID: 19706156; PMCID: PMC2738683.
    18. Zhang C, Kuspa A. Transcriptional down-regulation and rRNA cleavage in Dictyostelium discoideum mitochondria during Legionella pneumophila infection. PLoS One. 2009; 4(5):e5706. PMID: 19492077; PMCID: PMC2683564.
    19. Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski EA, Strassmann JE, Queller DC, Zupan B, Shaulsky G, Kuspa A. Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr Biol. 2009 Apr 14; 19(7):567-72. PMID: 19285397; PMCID: PMC2694408.
    20. Santorelli LA, Thompson CR, Villegas E, Svetz J, Dinh C, Parikh A, Sucgang R, Kuspa A, Strassmann JE, Queller DC, Shaulsky G. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature. 2008 Feb 28; 451(7182):1107-10. PMID: 18272966.
      View in: PubMed
    21. Katoh M, Chen G, Roberge E, Shaulsky G, Kuspa A. Developmental commitment in Dictyostelium discoideum. Eukaryot Cell. 2007 Nov; 6(11):2038-45. PMID: 17905919; PMCID: PMC2168402.
    22. Van Driessche N, Alexander H, Min J, Kuspa A, Alexander S, Shaulsky G. Global transcriptional responses to cisplatin in Dictyostelium discoideum identify potential drug targets. Proc Natl Acad Sci U S A. 2007 Sep 25; 104(39):15406-11. PMID: 17878305; PMCID: PMC2000517.
    23. Chen G, Zhuchenko O, Kuspa A. Immune-like phagocyte activity in the social amoeba. Science. 2007 Aug 3; 317(5838):678-81. PMID: 17673666; PMCID: PMC3291017.
    24. Sawai S, Guan XJ, Kuspa A, Cox EC. High-throughput analysis of spatio-temporal dynamics in Dictyostelium. Genome Biol. 2007; 8(7):R144. PMID: 17659086; PMCID: PMC2323234.
    25. Cabral M, Anjard C, Loomis WF, Kuspa A. Genetic evidence that the acyl coenzyme A binding protein AcbA and the serine protease/ABC transporter TagA function together in Dictyostelium discoideum cell differentiation. Eukaryot Cell. 2006 Dec; 5(12):2024-32. PMID: 17056744; PMCID: PMC1694806.
    26. Kuspa A, Loomis WF. The Genome of Dictyostelium discoideum. Methods Mol Biol. 2006; 346:15-30. PMID: 16957282.
      View in: PubMed
    27. Kuspa A. Restriction enzyme-mediated integration (REMI) mutagenesis. Methods Mol Biol. 2006; 346:201-9. PMID: 16957292.
      View in: PubMed
    28. Katoh M, Curk T, Xu Q, Zupan B, Kuspa A, Shaulsky G. Developmentally regulated DNA methylation in Dictyostelium discoideum. Eukaryot Cell. 2006 Jan; 5(1):18-25. PMID: 16400165; PMCID: PMC1360260.
    29. Song J, Xu Q, Olsen R, Loomis WF, Shaulsky G, Kuspa A, Sucgang R. Comparing the Dictyostelium and Entamoeba genomes reveals an ancient split in the Conosa lineage. PLoS Comput Biol. 2005 Dec; 1(7):e71. PMID: 16362072; PMCID: PMC1314882.
    30. Booth EO, Van Driessche N, Zhuchenko O, Kuspa A, Shaulsky G. Microarray phenotyping in Dictyostelium reveals a regulon of chemotaxis genes. Bioinformatics. 2005 Dec 15; 21(24):4371-7. PMID: 16234315.
      View in: PubMed
    31. Chen G, Kuspa A. Prespore cell fate bias in G1 phase of the cell cycle in Dictyostelium discoideum. Eukaryot Cell. 2005 Oct; 4(10):1755-64. PMID: 16215182; PMCID: PMC1265904.
    32. Eichinger L, Pachebat JA, Glöckner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A. The genome of the social amoeba Dictyostelium discoideum. Nature. 2005 May 5; 435(7038):43-57. PMID: 15875012; PMCID: PMC1352341.
    33. Van Driessche N, Demsar J, Booth EO, Hill P, Juvan P, Zupan B, Kuspa A, Shaulsky G. Epistasis analysis with global transcriptional phenotypes. Nat Genet. 2005 May; 37(5):471-7. PMID: 15821735.
      View in: PubMed
    34. Xu Q, Ibarra M, Mahadeo D, Shaw C, Huang E, Kuspa A, Cotter D, Shaulsky G. Transcriptional transitions during Dictyostelium spore germination. Eukaryot Cell. 2004 Oct; 3(5):1101-10. PMID: 15470238; PMCID: PMC522591.
    35. Knuth M, Khaire N, Kuspa A, Lu SJ, Schleicher M, Noegel AA. A novel partner for Dictyostelium filamin is an alpha-helical developmentally regulated protein. J Cell Sci. 2004 Oct 1; 117(Pt 21):5013-22. PMID: 15383615.
      View in: PubMed
    36. Maeda M, Lu S, Shaulsky G, Miyazaki Y, Kuwayama H, Tanaka Y, Kuspa A, Loomis WF. Periodic signaling controlled by an oscillatory circuit that includes protein kinases ERK2 and PKA. Science. 2004 May 7; 304(5672):875-8. PMID: 15131307.
      View in: PubMed
    37. Chen G, Shaulsky G, Kuspa A. Tissue-specific G1-phase cell-cycle arrest prior to terminal differentiation in Dictyostelium. Development. 2004 Jun; 131(11):2619-30. PMID: 15128662.
      View in: PubMed
    38. Zupan B, Bratko I, Demsar J, Juvan P, Curk T, Borstnik U, Beck JR, Halter J, Kuspa A, Shaulsky G. GenePath: a system for inference of genetic networks and proposal of genetic experiments. Artif Intell Med. 2003 Sep-Oct; 29(1-2):107-30. PMID: 12957783.
      View in: PubMed
    39. Good JR, Cabral M, Sharma S, Yang J, Van Driessche N, Shaw CA, Shaulsky G, Kuspa A. TagA, a putative serine protease/ABC transporter of Dictyostelium that is required for cell fate determination at the onset of development. Development. 2003 Jul; 130(13):2953-65. PMID: 12756178.
      View in: PubMed
    40. Sucgang R, Chen G, Liu W, Lindsay R, Lu J, Muzny D, Shaulsky G, Loomis W, Gibbs R, Kuspa A. Sequence and structure of the extrachromosomal palindrome encoding the ribosomal RNA genes in Dictyostelium. Nucleic Acids Res. 2003 May 1; 31(9):2361-8. PMID: 12711681; PMCID: PMC154234.
    41. Zupan B, Demsar J, Bratko I, Juvan P, Halter JA, Kuspa A, Shaulsky G. GenePath: a system for automated construction of genetic networks from mutant data. Bioinformatics. 2003 Feb 12; 19(3):383-9. PMID: 12584124.
      View in: PubMed
    42. Taminato A, Bagattini R, Gorjão R, Chen G, Kuspa A, Souza GM. Role for YakA, cAMP, and protein kinase A in regulation of stress responses of Dictyostelium discoideum cells. Mol Biol Cell. 2002 Jul; 13(7):2266-75. PMID: 12134067; PMCID: PMC117311.
    43. Van Driessche N, Shaw C, Katoh M, Morio T, Sucgang R, Ibarra M, Kuwayama H, Saito T, Urushihara H, Maeda M, Takeuchi I, Ochiai H, Eaton W, Tollett J, Halter J, Kuspa A, Tanaka Y, Shaulsky G. A transcriptional profile of multicellular development in Dictyostelium discoideum. Development. 2002 Apr; 129(7):1543-52. PMID: 11923193.
      View in: PubMed
    44. Wang B, Kuspa A. CulB, a putative ubiquitin ligase subunit, regulates prestalk cell differentiation and morphogenesis in Dictyostelium spp. Eukaryot Cell. 2002 Feb; 1(1):126-36. PMID: 12455979; PMCID: PMC118045.
    45. Kuspa A, Sucgang R, Shaulsky G. The promise of a protist: the Dictyostelium genome project. Funct Integr Genomics. 2001 Sep; 1(5):279-93. PMID: 11793247.
      View in: PubMed
    46. Demsar J, Zupan B, Bratko I, Kuspa A, Halter JA, Beck RJ, Shaulsky G. GenePath: a computer program for genetic pathway discovery from mutant data. Stud Health Technol Inform. 2001; 84(Pt 2):956-9. PMID: 11604873.
      View in: PubMed
    47. Wessels DJ, Zhang H, Reynolds J, Daniels K, Heid P, Lu S, Kuspa A, Shaulsky G, Loomis WF, Soll DR. The internal phosphodiesterase RegA is essential for the suppression of lateral pseudopods during Dictyostelium chemotaxis. Mol Biol Cell. 2000 Aug; 11(8):2803-20. PMID: 10930471; PMCID: PMC14957.
    48. Sucgang R, Shaulsky G, Kuspa A. Toward the functional analysis of the Dictyostelium discoideum genome. J Eukaryot Microbiol. 2000 Jul-Aug; 47(4):334-9. PMID: 11140446.
      View in: PubMed
    49. Good JR, Kuspa A. Evidence that a cell-type-specific efflux pump regulates cell differentiation in Dictyostelium. Dev Biol. 2000 Apr 1; 220(1):53-61. PMID: 10720430.
      View in: PubMed
    50. Souza GM, da Silva AM, Kuspa A. Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development. 1999 Jun; 126(14):3263-74. PMID: 10375515.
      View in: PubMed
    51. Wang B, Shaulsky G, Kuspa A. Multiple developmental roles for CRAC, a cytosolic regulator of adenylyl cyclase. Dev Biol. 1999 Apr 1; 208(1):1-13. PMID: 10075837.
      View in: PubMed
    52. Loomis WF, Kuspa A, Shaulsky G. Two-component signal transduction systems in eukaryotic microorganisms. Curr Opin Microbiol. 1998 Dec; 1(6):643-8. PMID: 10066536.
      View in: PubMed
    53. Rivero F, Kuspa A, Brokamp R, Matzner M, Noegel AA. Interaptin, an actin-binding protein of the alpha-actinin superfamily in Dictyostelium discoideum, is developmentally and cAMP-regulated and associates with intracellular membrane compartments. J Cell Biol. 1998 Aug 10; 142(3):735-50. PMID: 9700162; PMCID: PMC2148174.
    54. Souza GM, Lu S, Kuspa A. YakA, a protein kinase required for the transition from growth to development in Dictyostelium. Development. 1998 Jun; 125(12):2291-302. PMID: 9584128.
      View in: PubMed
    55. Wang B, Kuspa A. Dictyostelium development in the absence of cAMP. Science. 1997 Jul 11; 277(5323):251-4. PMID: 9211856.
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    56. Kuspa A, Loomis WF. Ordered yeast artificial chromosome clones representing the Dictyostelium discoideum genome. Proc Natl Acad Sci U S A. 1996 May 28; 93(11):5562-6. PMID: 8643615; PMCID: PMC39286.
    57. Xu XS, Kuspa A, Fuller D, Loomis WF, Knecht DA. Cell-cell adhesion prevents mutant cells lacking myosin II from penetrating aggregation streams of Dictyostelium. Dev Biol. 1996 May 1; 175(2):218-26. PMID: 8626027.
      View in: PubMed
    58. Kuspa A, Dingermann T, Nellen W. Analysis of gene function in Dictyostelium. Experientia. 1995 Dec 18; 51(12):1116-23. PMID: 8536799.
      View in: PubMed
    59. Loomis WF, Welker D, Hughes J, Maghakian D, Kuspa A. Integrated maps of the chromosomes in Dictyostelium discoideum. Genetics. 1995 Sep; 141(1):147-57. PMID: 8536963; PMCID: PMC1206713.
    60. Shaulsky G, Kuspa A, Loomis WF. A multidrug resistance transporter/serine protease gene is required for prestalk specialization in Dictyostelium. Genes Dev. 1995 May 1; 9(9):1111-22. PMID: 7744252.
      View in: PubMed
    61. Segall JE, Kuspa A, Shaulsky G, Ecke M, Maeda M, Gaskins C, Firtel RA, Loomis WF. A MAP kinase necessary for receptor-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol. 1995 Feb; 128(3):405-13. PMID: 7844154; PMCID: PMC2120359.
    62. Kuspa A, Loomis WF. REMI-RFLP mapping in the Dictyostelium genome. Genetics. 1994 Nov; 138(3):665-74. PMID: 7851764; PMCID: PMC1206217.
    63. He Q, Chen H, Kuspa A, Cheng Y, Kaiser D, Shimkets LJ. A physical map of the Myxococcus xanthus chromosome. Proc Natl Acad Sci U S A. 1994 Sep 27; 91(20):9584-7. PMID: 7937810; PMCID: PMC44857.
    64. Titus MA, Kuspa A, Loomis WF. Discovery of myosin genes by physical mapping in Dictyostelium. Proc Natl Acad Sci U S A. 1994 Sep 27; 91(20):9446-50. PMID: 7937787; PMCID: PMC44829.
    65. Insall R, Kuspa A, Lilly PJ, Shaulsky G, Levin LR, Loomis WF, Devreotes P. CRAC, a cytosolic protein containing a pleckstrin homology domain, is required for receptor and G protein-mediated activation of adenylyl cyclase in Dictyostelium. J Cell Biol. 1994 Sep; 126(6):1537-45. PMID: 8089184; PMCID: PMC2290948.
    66. Dynes JL, Clark AM, Shaulsky G, Kuspa A, Loomis WF, Firtel RA. LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium. Genes Dev. 1994 Apr 15; 8(8):948-58. PMID: 7926779.
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    67. Loomis WF, Kuspa A, Shaulsky G. Gene discovery in Dictyostelium. Genet Eng (N Y). 1994; 16:49-64. PMID: 7765201.
      View in: PubMed
    68. Kuspa A, Plamann L, Kaiser D. A-signalling and the cell density requirement for Myxococcus xanthus development. J Bacteriol. 1992 Nov; 174(22):7360-9. PMID: 1429458; PMCID: PMC207432.
    69. Kuspa A, Loomis WF. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc Natl Acad Sci U S A. 1992 Sep 15; 89(18):8803-7. PMID: 1326764; PMCID: PMC50009.
    70. Kuspa A, Maghakian D, Bergesch P, Loomis WF. Physical mapping of genes to specific chromosomes in Dictyostelium discoideum. Genomics. 1992 May; 13(1):49-61. PMID: 1577493.
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    71. Plamann L, Kuspa A, Kaiser D. Proteins that rescue A-signal-defective mutants of Myxococcus xanthus. J Bacteriol. 1992 May; 174(10):3311-8. PMID: 1577696; PMCID: PMC206000.
    72. Kuspa A, Plamann L, Kaiser D. Identification of heat-stable A-factor from Myxococcus xanthus. J Bacteriol. 1992 May; 174(10):3319-26. PMID: 1577697; PMCID: PMC206001.
    73. Kim SK, Kaiser D, Kuspa A. Control of cell density and pattern by intercellular signaling in Myxococcus development. Annu Rev Microbiol. 1992; 46:117-39. PMID: 1444251.
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    80. Kroos L, Kuspa A, Kaiser D. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol. 1986 Sep; 117(1):252-66. PMID: 3017794.
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    81. Kaiser D, Kroos L, Kuspa A. Cell interactions govern the temporal pattern of Myxococcus development. Cold Spring Harb Symp Quant Biol. 1985; 50:823-30. PMID: 3007019.
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    82. Loomis WF, Kuspa A. Biochemical and genetic analysis of pre-stalk specific acid phosphatase in Dictyostelium. Dev Biol. 1984 Apr; 102(2):498-503. PMID: 6706012.
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