Gastrointestinal epithelium is an early extrathymic site for increased prevalence of CD34+ progenitor cells in contrast to the thymus during primary simian immunodeficiency virus infection

Journal of Virology

Volumn 73, Issue 5, 1999, Pages 4518-4523

  Mattapallil, Joseph J ^a   Smit McBride, Zeljka ^a   Dandekar, Satya ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD4 ANTIGEN; THY 1 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOGENESIS; INTESTINE MUCOSA; LYMPHOPOIESIS; MONKEY DISEASE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; T LYMPHOCYTE;

EID: 0032930745     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.5.4518-4523.1999     Document Type: Article

References (57)

1. Adleman, L. M., and D. Wofsy. 1993. T-cell homeostasis: implications in HIV infection. J. Acquired Immune Defic. Syndr. 6:144-152.
2. Bagnara, G. P., G. Zauli, M. Giovannini, M. C. Re, G. Furlini, and M. La Placa. 1990. Early loss of circulating hemopoietic progenitors in HIV-1-infected subjects. Exp. Hematol. (New York) 18:426-430.
3. Baskin, G. B., M. Murphey-Corb, L. N. Martin, B. Davison-Fairburn, F. S. Hu, and D. Kuebler. 1991. Thymus in simian immunodeficiency virus-infected rhesus monkeys, Lab. Investig. 65:400-407.
4. Baum, C. M., I. L. Weissman, A. S. Tsukamoto, A. M. Buckle, and B. Peault. 1992. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. USA 89:2804-2808.
5. Berenson, R. J., R. G. Andrews, W. I. Bensinger, D. Kalamasz, G. Knitter, C. D. Buckner, and I. D. Bernstein. 1988. Antigen CD34+ marrow cells engraft lethally irradiated baboons. J. Clin. Investig. 81:951-955.
6. Berenson, R. J., W. I. Bensinger, R. S. Hill, R. G. Andrews, J. Garcia-Lopez, D. F. Kalamasz, B. J. Still, G. Spitzer, C. D. Buckner, I. D. Bernstein, et al. 1991. Engraftment after infusion of CD34+ marrow cells in patients with breast cancer or neuroblastoma. Blood 77:1717-1722.
7. Brandt, J., R. A. Briddell, E. F. Srour, T. B. Leemhuis, and R. Hoffman. 1992. Role of c-kit ligand in the expansion of human hematopoietic progenitor cells. Blood 79:634-641.
8. Briddell, R. A., V. C. Broudy, E. Bruno, J. E. Brandt, E. F. Srour, and R. Hoffman. 1992. Further phenotypic characterization and isolation of human hemalopoietic progenitor cells using a monoclonal antibody to the c-kit receptor. Blood 79:3159-3167.
9. Briddell, R. A., E. Bruno, R. J. Cooper, J. E. Brandt, and R. Hoffman. 1991. Effect of c-kit ligand on in vitro human megakaryocytopoiesis. Blood 78: 2854-2859.
10. Civin, C., T. T. M. Fackler, I. Bernstein, H. Buhring, L. Campos, M. F. Greaves, M. Kamoun, D. Katz, P. Landsorp, T. Look, B. Seed, D. R. Sutherland, R. Tindle, and B. Vchanska-Ziegler. 1989. Summary of CD34 cluster workshop section, p. 818-825. In Leukocyte typing IV. Oxford University Press, Oxford, United Kingdom.
11. Civin, C. I., L. C. Strauss, C. Brovall, M. J. Fackler, J. F. Schwartz, and J. H. Shaper. 1984. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J. Immunol. 133:157-165.
12. Craig, W., R. Kay, R. L. Cutler, and P. M. Lansdorp. 1993. Expression of Thy-1 on human hematopoietic progenitor cells. J. Exp. Med. 177:1331-1342.
13. Deichmann, M., R. Kronenwett, and R. Haas. 1997. Expression of the human immunodeficiency virus type-1 coreceptors CXCR-4 (fusin, LESTR) and CKR-5 in CD34+ hematopoietic progenitor cells. Blood 89:3522-3528.
14. De Luca, A., L. Teofili, A. Antinori, M. S. Iovino, P. Mencarini, E. Visconti, E. Tamburrini, G. Leone, and L. Ortona. 1993. Haemopoietic CD34+ progenitor cells are not infected by HIV-1 in vivo but show impaired clonogenesis. Br. J. Haematol. 85:20-24.
15. Donahue, R. E., M. M. Johnson, L. I. Zon, S. C. Clark, and J. E. Groopman. 1987. Suppression of in vitro haematopoiesis following human immunodeficiency virus infection. Nature 326:200-203.
16. Ganser, A., O. G. Ottmann, H. von Briesen, B. Volkers, H. Rubsamen-Waigmann, and D. Hoelzer. 1990. Changes in the haematopoietic progenitor cell compartment in the acquired immunodeficiency syndrome. Res. Virol. 141:185-193.
17. Guy-Grand, D., N. Cerf-Bensussan, B. Malissen, M. Malassis-Seris, C. Briottet, and P. Vassalli. 1991. Two gut intraepithelial CD8+ lymphocyte populations with different T cell receptors: a role for the gut epithelium in T cell differentiation. J. Exp. Med. 173:471-481.
18. Haas, R., R. Mohle, M. Pforsich, S. Fruehauf, B. Witt, H. Goldschmidt, and W. Hunstein. 1995. Blood-derived autografts collected during granulocyte colony-stimulating factor-enhanced recovery are enriched with early Thy-1 + hematopoietic progenitor cells. Blood 85:1936-1943.
19. Harris, M., P. Patenaude, P. Cooperberg, D. Filipenko, A. Thorne, J. Raboud, S. Rae, P. Dailey, D. Chernoff, J. Todd, B. Conway, and J. S. Montaner. 1997. Correlation of virus load in plasma and lymph node tissue in human immunodeficiency virus infection. INCAS Study Group. Italy, The Netherlands, Canada, Australia, and (United) States. J. Infect. Dis. 176: 1388-1392.
20. Heise, C., C. J. Miller, A. Lackner, and S. Dandekar. 1994. Primary acute simian immunodeficiency virus infection of intestinal lymphoid tissue is associated with gastrointestinal dysfunction. J. Infect. Dis. 169:1116-1120.
21. Heise, C., P. Vogel, C. J. Miller, A. Lackner, and S. Dandekar. 1993. Distribution of SIV infection in the gastrointestinal tract of rhesus macaques at early and terminal stages of AIDS. J. Med. Primatol. 22:187-193.
22. Hillyer, C. D., D. A. D. Lackey, F. Villinger, E. F. Winton, H. M. McClure, and A. A. Ansari. 1993. CD34+ and CFU-GM progenitors are significantly decreased in SIVsmm9 infected rhesus macaques with minimal evidence of direct viral infection by polymerase chain reaction. Am. J. Hematol. 43:274-278.
23. Jenkins, M., M. B. Hanley, M. B. Moreno, E. Wieder, and J. M. McCune. 1998. Human immunodeficiency virus-1 infection interrupts thymopoiesis and multilineage hematopoiesis in vivo. Blood 91:2672-2678.
24. Kanamori, Y., K. Ishimaru, M. Nanno, K. Maki, K. Ikuta, H. Nariuchi, and H. Ishikawa. 1996. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit+ IL-7R+ Thy1+ lympho-hemopoietic progenitors develop. J. Exp. Med. 184:1449-1459.
25. Klimpel, G. R., K. E. Langley, J. Wypych, J. S. Abrams, A. K. Chopra, and D. W. Niesel. 1996. A role for stem cell factor (SCF): c-kit interaction(s) in the intestinal tract response to Salmonella typhimurium infection. J. Exp. Med. 184:271-276.
26. Koka, P. S., J. K. Fraser, Y. Bryson, G. C. Bristol, G. M. Aldrovandi, E. S. Daar, and J. A. Zack. 1998. Human immunodeficiency virus inhibits multi-lineage hematopoiesis in vivo. J. Virol. 72:5121-5127.
27. Kourtis, A. P., C. Ibegbu, A. J. Nahmias, F. K. Lee, W. S. Clark, M. K. Sawyer, and S. Nesheim. 1996. Early progression of disease in HIV-infected infants with thymus dysfunction. N. Engl. J. Med. 335:1431-1436. (Erratum, 336:595, 1997.)
28. Louache, F., N. Debili, A. Marandin, L. Coulombel, and W. Vainchenker. 1994. Expression of CD4 by human hematopoietic progenitors. Blood 84: 3344-3355.
29. Lunardi-Iskandar, Y., M. T. Nugeyre, V. Georgoulias, F. Barre-Sinoussi, C. Jasmin, and J. C. Chermann. 1989. Replication of the human immunodeficiency virus 1 and impaired differentiation of T cells after in vitro infection of bone marrow immature T cells. J. Clin. Investig. 83:610-615.
30. Lundqvist, C., V. Baranov, S. Hammarstrom, L. Athlin, and M. L. Hammarstrom. 1995. Intra-epithelial lymphocytes. Evidence for regional specialization and extrathymic T cell maturation in the human gut epithelium. Int. Immunol. 7:1473-1487.
31. Manegold, C., H. Jablonowski, C. Armbrecht, G. Strohmeyer, and T. Pietsch. 1995. Serum levels of stem cell factor are increased in asymptomatic human immunodeficiency virus-infected patients and are associated with prolonged survival. Blood 86:243-249.
32. Marandin, A., A. Katz, E. Oksenhendler, M. Tulliez, F. Picard, W. Vainchenker, and F. Louache. 1996. Loss of primitive hematopoietic progenitors in patients with human immunodeficiency virus infection. Blood 88:4568-4578.
33. Margolick, J. B., A. D. Donnenberg, A. Munoz, L. P. Park, K. D. Bauer, J. V. Giorgi, J. Ferbas, and A. J. Saah. 1993. Changes in T and non-T lymphocyte subsets following seroconversion to HIV-1: stable CD3+ and declining CD3- populations suggest regulatory responses linked to loss of CD4 lymphocytes. The Multicenter AIDS Cohort Study. J. Acquired Immune Defic. Syndr. 6:153-161.
34. + T-cell depletion in primary simian immunodeficiency virus infection. J. Virol. 72:6421-6429.
35. Miles, S. A., K. Lee, L. Hutlin, K. M. Zsebo, and R. T. Milsuyasu. 1991. Potential use of human stem cell factor as adjunctive therapy for human immunodeficiency virus-related cytopenias. Blood 78:3200-3208.
36. Mosley, R. L., and J. R. Klein. 1992. Peripheral engraftment of fetal intestine into athymic mice sponsors T cell development: direct evidence for thymopoietic function of murine small intestine. J. Exp. Med. 176:1365-1373.
37. Muller, J. G., V. Krenn, S. Czub, C. Stahl-Hennig, C. Coulibaly, G. Hunsmann, and H. K. Muller-Hermelink. 1993. The thymic epithelial reticulum and interdigitating cells in SIV-induced thymus atrophy and its comparison with other forms of thymus involution. Res. Virol. 144:93-98.
38. Muller, J. G., V. Krenn, C. Schindler, S. Czub, C. Stahl-Hennig, C. Coulibaly, G. Hunsmann, C. Kneitz, T. Kerkau, A. Rethwilm, et al. 1993. Alterations of thymus cortical epithelium and interdigitating dendritic cells but no increase of thymocyte cell death in the early course of simian immunodeficiency virus infection. Am. J. Pathol. 143:699-713.
39. Murray, L., B. Chen, A. Galy, S. Chen, R. Tushinski, N. Uchida, R. Negrin, G. Tricot, S. Jagannath, D. Vesole, et al. 1995. Enrichment of human hematopoietic stem cell activity in the CD34+Thy-1+Lin- subpopulation from mobilized peripheral blood. Blood 85:368-378.
40. Pachl, C., J. A. Todd, D. G. Kern, P. J. Sheridan, S. J. Fong, M. Stempien, B. Hoo, D. Besemer, T. Yeghiazarian, B. Irvine, et al. 1995. Rapid and precise quantification of HIV-1 RNA in plasma using a branched DNA signal amplification assay. J. Acquired Immune Defic. Syndr. Hum. Retro-virol. 8:446-454.
41. Poussier, P., and M. Julius. 1995. T-cell development and selection in the intestinal epithelium. Semin. Immunol. 7:321-334.
42. Poussier, P., and M. Julius. 1994. Thymus independent T cell development and selection in the intestinal epithelium. Annu. Rev. Immunol. 12:521-553.
43. Puddington, L., S. Olson, and L. Lefrancois. 1994. Interactions between stem cell factor and c-Kit are required for intestinal immune system homeostasis. Immunity 1:733-739.
44. Rosenzweig, M., D. P. Clark, and G. N. Gaulton. 1993. Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS 7:1601-1605.
45. Saito, H., Y. Kanamori, T. Takemori, H. Nariuchi, E. Kubota, H. Takahashi-Iwanaga, T. Iwanaga, and H. Ishikawa. 1998. Generation of intestinal T cells from progenitors residing in gut cryptopatches. Science 280:275-278.
46. + T-cell depletion at all stages of simian immunodeficiency virus infection compared to peripheral lymphocytes. J. Virol. 72:6646-6656.
47. Stanley, S. K., J. M. McCune, H. Kaneshima, J. S. Justement, M. Sullivan, E. Boone, M. Baseler, J. Adelsberger, M. Bonyhadi, J. Orenstein, et al. 1993. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID-hu mouse. J. Exp. Med. 178:1151-1163.
48. Stella, C. C., A. Ganser, and D. Hoelzer. 1987. Defective in vitro growth of the hemopoietic progenitor cells in the acquired immunodeficiency syndrome. J. Clin. Investig. 80:286-293.
49. Stone, J. D., C. C. Heise, D. R. Canfield, M. J. Elices, and S. Dandekar. 1995. Differences in viral distribution and cell adhesion molecule expression in the intestinal tract of rhesus macaques infected with pathogenic and nonpathogenic SIV. J. Med. Primatol. 24:132-140.
50. Sutherland, D. R., and A. Keating. 1992. The CD34 antigen: structure, biology, and potential clinical applications. J. Hematother. 1:115-129.
51. Veazey, R. S., M. DeMaria, L. V. Chalifoux, D. E. Shvetz, D. R. Pauley, H. L. Knight, M. Rosenzweig, P. R. Johnson, C. R. Desrosiers, and A. A. Lackner. 1998. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280:427-431.
52. Weinberg, R. S., E. D. Chusid, Y. Galperin, J. C. Thomson, T. Cheung, and H. S. Sacks. 1998. Effect of antiviral drugs and hematopoietic growth factors on in vitro erythropoiesis. Mt. Sinai J. Med. 65:5-13.
53. Wineman, J. P., G. L. Gilmore, C. Gritzmacher, B. E. Torbett, and C. E. Muller-Sieburg. 1992. CD4 is expressed on murine pluripotent hematopoietic stem cells. Blood 80:1717-1724.
54. Wu, L., R. Scollay, M. Egerton, M. Pearse, G. J. Spangrude, and K. Shortman. 1991. CD4 expressed on earliest T-lineage precursor cells in the adult murine thymus. Nature 349:71-74.
55. Wykrzykowska, J. J., M. Rosenzweig, R. S. Veazey, M. A. Simon, K. Halvorsen, R. C. Desrosiers, R. P. Johnson, and A. A. Lackner. 1998. Early regeneration of thymic progenitors in rhesus macaques infected with simian immunodeficiency virus. J. Exp. Med. 187:1767-1778.
56. Zauli, G., M. C. Re, B. Davis, L. Sen, G. Visani, L. Gugliotta, G. Furlini, and M. La Placa. 1992. Impaired in vitro growth of purified (CD34+) hematopoietic progenitors in human immunodeficiency virus-1 seropositive thrombocytopenic individuals. Blood 79:2680-2687.
57. Zauli, G., M. C. Re, G. Visani, G. Furlini, P. Mazza, M. Vignoli, and M. La Placa. 1992. Evidence for a human immunodeficiency virus type 1-mediated suppression of uninfected hematopoietic (CD34+) cells in AIDS patients. J. Infect. Dis. 166:710-716.