medigraphic.com
ISSN 0187-5337 (Print)
Instituto Nacional de Perinatología

2013, Number 1

<< Back Next >>

Perinatol Reprod Hum 2013; 27 (1)

Relationship between male infertility and genitourinary mycoplasma infection. An update

Díaz-García FJ, Flores-Medina S,

Language: Spanish
References: 114
Page: 21-34
PDF size: 325.77 Kb.


ABSTRACT

It has been suggested for more than 30 years that seminal infections caused by mycoplasmas provoke impairment of the human sperm functionality. However, the studies have shown conflicting results. This review presents recent evidence from in vitro studies that confirm adherence and invasiveness toward human spermatozoa by Mycoplasma hominis, Ureaplasma urealyticum, U. parvum and M. genitalium. We discuss how those infections can cause: a) sperm oxidative stress; b) disruption of energy production mechanisms that lead to impaired sperm motility and viability; c) disturbance of nuclear and cellular organization by effect of bacterial endonucleases, phospholipases and aminopeptidases; d) masking of chemotactic receptors and obstruction of fertilization, and e) compromise of sperm’s membrane integrity, with exposure of self-antigens and auto-immune responses.


REFERENCES

  1. Makar RS, Toth TL. The evaluation of infertility. Am J Clin Pathol 2002; 117: S95-S103.

  2. Forti G, Krausz C. Clinical review 100: evaluation and treatment of the infertile couple. J Clin Endocrinol Metabol 1998; 83: 4177-88.

  3. Gdoura R, Kchaou W, Chaari C, Znazen A, Keskes L, Rebai T et al. Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis and Mycoplasma genitalium infections and semen quality of infertile men. BMC Infect Dis 2007; 7: 129.

  4. Gdoura R, Kchaou W, Ammar-Keskes L, Chakroun N, Sellemi A, Znazen A et al. Assessment of Chlamydia trachomatis, Ureaplasma urealyticum, Ureaplasma parvum, Mycoplasma hominis, and Mycoplasma genitalium in semen and first void urine specimens of asymptomatic male partners of infertile couples. J Androl 2008; 29: 198-206.

  5. Robertson JA, Stemke GW, Davis Jr JA, Harasawa R, Thirkell D, Kong F et al. Proposal of Ureaplasma parvum sp. nov. and emended description of Ureaplasma urealyticum. Int J Syst Evol Microbiol 2002; 52: 587-97.

  6. Styler M, Shapiro SS. Mollicutes (mycoplasma) in infertility. Fertil Steril 1985; 44: 1-11.

  7. Svenstrup HF, Fedder J, Abraham-Peskir J, Birkelund S, Christiansen G. Mycoplasma genitalium attaches to human spermatozoa. Hum Reprod 2003; 18: 2103-09.

  8. Cassell GH, Blanchard A, Duffy L, Crabb D, Waites KB. Mycoplasmas. In: Howard BJ, Keiser JF, Weissfeld AS, Smith TF, Tilton RC, editors. Clinical and Pathogenic Microbiology. USA: Mosby; 1993. p. 491-502.

  9. Gilbert GI, Weisberg E. Infertility as an infectious disease —epidemiology and prevention—. Bailliere’s Clin Obstet Gynaecol 1993; 7: 159-81.

  10. Cassell GH, Cole BC. Mycoplasmas as agents of human disease. N Engl J Med 1981; 304: 80-89.

  11. Jensen JS. Mycoplasma genitalium infections. Dan Med Bull 2006; 53: 1-27.

  12. McCormack WM. Ureaplasma urealyticum: ecologic niche and epidemiologic considerations. Pediatr Infect Dis 1986; 5: S232-33.

  13. Tully JG. Current status of the mollicute flora of humans. Clin Infect Dis 1993; 17: S2-9.

  14. Andrade-Rocha FT. Ureaplasma urealyticum and Mycoplasma hominis in men attending for routine semen analysis. Prevalence, incidence by age and clinical settings, influence on sp.erm characteristics, relationship with the leukocyte count and clinical value. Urol Int 2003; 71: 377-81.

  15. Bornman MS, Mahomed MF, Boomker D, Schulenburg GW, Reif S, Crewe-Brown HH. Microbial flora in semen of infertile African men at Garankuwa Hospital. Andrologia 1990; 22: 118-21.

  16. de Jong Z, Plante F, Prie N, Talazae N, Nabsat A, Chabanon G. Comparison of the incidence of Ureaplasma urealyticum in infertile men and in donors of semen. Eur Urol 1990; 18: 127-31.

  17. Busolo F, Zanchetta R. The effect of Mycoplasma hominis and Ureaplasma urealyticum on hamster egg in vitro penetration by human spermatozoa. Fertil Steril 1985; 43: 110-14.

  18. Busolo F, Zanchetta R, Bertolini G. Mycoplasmic localization patterns on spermatozoa from infertile men. Fertil Steril 1984; 42: 412-17.

  19. Busolo F, Zanchetta R, Lanzone E, Casinato R. Microbial flora in semen of asymptomatic infertile men. Andrologia 1984; 16: 269-75.

  20. Fowlkes DM, MacLeod J, O’Leary WM. T-mycoplasma and human infertility: correlation of infection with alterations in seminal parameters. Fertil Steril 1975; 26: 1212-18.

  21. Naessens A, Foulon W, Debruker P, Lauwers S. Recovery of microrganisms in semen and relationship in semen evaluation. Fertil Steril 1986, 45: 101-5.

  22. Nuñez-Calonge R, Caballero P, Redondo C, Baquero F, Martínez-Ferrer M, Meseguer MA. Ureaplasma urealyticum reduces motility and induces membrane alterations in human spermatozoa. Hum Reprod 1998; 13: 2756-61.

  23. Rose BI, Scott BS. Sperm motility, morphology, hyperaction, and ionophore-induced acromosome reactions after overnight incubation with mycoplasmas. Fertil Steril 1994; 61: 341-48.

  24. Sanchez R, Hein R, Concha M, Virgil P, Schill WB. Mollicutes in male infertily; is antibiotic therapy indicated? Andrologia 1990; 22: 355-60.

  25. Upadhyaya M, Hibbard BM, Walker SM. The effect of Ureaplasma urealyticum on semen characteristics. Fertil Steril 1984; 41: 304-8.

  26. Xu C, Sun GF, Zhu YF. The correlation of Ureaplasma urealyticum infection with infertility. Andrologia 1997; 29: 219-26.

  27. Soffer Y, Herman A, Ron-El R, Caspi E, Golan A, Samra Z. Male genital mycoplasmas and Chlamydia trachomatis culture: its relationships with accessory gland function, sperm quality, and autoimmunity. Fertil Steril 1990; 53: 331-36.

  28. Swenson CE, Toth A, O’Leary WM. Ureaplasma urealyticum and human infertility: the effect of antibiotic therapy on semen quality. Fertil Steril 1979; 31: 660-5.

  29. Toth A, Lesser ML, Brooks C, Labriola D. Subsequent pregnancies among 161 couples treated for T-mycoplasma genital-tract infection. New Engl J Med 1983; 308: 505-7.

  30. Montagut JM, Lapretre S, Degoy J, Rousseau M. Ureaplasma in semen and IVF. Human Reprod 1991; 6: 727-29.

  31. Hill AC, Tucker MJ, Whittingham DG, Craft I. Mycoplasma and in vitro fertilization. Fertil Steril 1987; 47: 652-55.

  32. Toth A, Swenson CE, O’Leary WM. Light microscopy an aid in predicting Ureaplasma infection in human semen. Fertil Steril 1978; 30, 586-91.

  33. Levy R, Layani-Milon MP, Giscard-D’Estaing S, Najioullah F, Lornage J, Aymard M et al. Screening for Chlamydia trachomatis and Ureaplasma urealyticum infection in semen from asymptomatic male partners of infertile couples prior to in vitro fertilization. Int J Androl 1999; 22: 113-18.

  34. Knox CL, Allan JA, Allan JM, Edirisinghe WR, Stenzel D, Lawrence FA et al. Ureaplasma parvum and Ureaplasma urealyticum are detected in semen after washing before assisted reproductive technology procedures. Fertil Steril 2003; 80: 921-29.

  35. Sanocka-Maciejewska D, Ciupińska M, Kurpisz M. Bacterial infection and semen quality. J Reprod Immunol 2005; 67: 51-56.

  36. Wang Y, Liang CL, Wu JQ, Xu C, Qin SX, Gao ES. Do Ureaplasma urealyticum infections in the genital tract affect semen quality? Asian J Androl 2006; 8: 562-68.

  37. Eggert-Kruse W, Kiefer I, Beck C, Demirakca T, Strowitzki T. Role of tumor necrosis factor alpha (TNF-α) and interleukin 1-beta (IL-1β) determination in seminal plasma during infertility investigation. Fertil Steril 2007; 87: 810-23.

  38. Golshani M, Eslami G, Ghobadloo SM, Fallah F, Goudarzi H, Rahbar AAS et al. Detection of Chlamydia trachomatis, Mycoplasma hominis and Ureaplasma urealyticum by multiplex PCR in semen sample of infertile men. Ir J Public Health 2007; 36: 50-57.

  39. Zinzendorf NY, Kouassi-Agbessi BT, Lathro JS, Don C, Kouadio L, Loukou YG. Ureaplasma urealyticum or Mycoplasma hominis infections and semen quality of infertile men in Abidjan. J Reprod Contracep 2008; 19: 65-72.

  40. Al-Daghistani HI, Abdel-Dayem M. Clinical significance of asymptomatic urogenital Mycoplasma hominis and Ureaplasma urealyticum in relation to seminal fluid parameters among infertile Jordanian males. Middle East Fertil Soc J 2010; 15: 29-34.

  41. Ahmadi MH, Amirmozafari N, Kazemi B, Sadighi-Gilani MA, Jazi FM. Use of PCR to detect Mycoplasma hominis and Ureaplasma urealyticum from semen samples of infertile men who referred to Royan Institute in 2009. Yakhteh Med J 2010; 12: 371-80.

  42. Salmeri M, Valenti D, La Vignera S, Bellanca S, Maello A, Toscano MA et al. Prevalence of Ureaplasma urealyticum and Mycoplasma hominis infection in unselected infertile men. J. Chemother 2012; 24: 81-86.

  43. Baseman JB, Tully JG. Mycoplasmas: sophisticated reemerging and burdened by their notoriety. Emerging Infect Dis 1997; 3: 21-32.

  44. Razin S, Yoguev D, Naot Y. Molecular biology and pathogenicity of mycoplasmas. Microbiol Mol Biol Rev 1998; 162: 1094-156.

  45. Razin S. Peculiar properties of mycoplasmas: the smallest self-replicating prokariotes. FEMS Microbiol Lett 1992; 100: 423-32.

  46. Taylor-Robinson D. Infections due to species of Mycoplasma and Ureaplasma: an update. Clin Infect Dis 1996; 23: 671-84.

  47. Waites KB, Bébéar CM, Robertson JA, Talkington DF, Kenny GE. 2001. Cumitech 34, Laboratory diagnosis of mycoplasmal infections. Coordinating ed., F. S. Nolte. Washington, D.C.: American Society for Microbiology, 2001.

  48. Andreev J, Borovsky Z, Rosenshine I, Rottem S. Invasion of HeLa cells by Mycoplasma penetrans and the induction of tyrosine phosphorylation of a 145 kDa host cell protein. FEMS Microbiol Lett 1995; 132: 189-94.

  49. Baseman JB, Lange M, Criscimagna NL, Giron JA, Thomas CA. Interplay between Mycoplasmas and host target cells. Microb Pathog 1995; 19: 105-16.

  50. Díaz-García FJ, Herrera-Mendoza AP, Giono-Cerezo S, Guerra-Infante F. Mycoplasma hominis attaches to and locates intracellularly on human spermatozoa. Hum Reprod 2006; 21: 1591-98.

  51. Girón JA, Lange M, Baseman JB. Adherence, fibronectin binding, and induction of cytoskeleton reorganization in cultured human cells by Mycoplasma penetrans. Infect Immun 1996; 64: 197-208.

  52. Jensen JS, Blom J, Lind K. Intracellular location of Mycoplasma genitalium in cultured Vero cells as demonstrated by electron microscopy. Int J Exp Path 1994; 75: 91-98.

  53. Lo SC, Hayes MM, Kotani H. Adhesion onto and invasion into mammalian cells by Mycoplasma penetrans -A newly isolated mycoplasma from patients with AIDS. Mod Pathol 1993; 6: 276-80.

  54. Taylor-Robinson D, Davies HA, Sarathchandra P, Furr PM. Intracellular location of Mycoplasmas in cultured cells demonstrated by immunocytochemistry and electron microscopy. Int J Exp Pathol 1991; 72: 705-14.

  55. Bové JM. Molecular features of Mollicutes. Clin Infect Dis 1993; 17: S10-31.

  56. Chambaud I, Wróblewski H, Blanchard A. Interactions between mycoplasma lipoproteins and the host immune system. Trends Microbiol 1999; 7: 493-99.

  57. Momynaliev KT, Govorun VM. Mechanisms of genetic instability in Mollicutes (mycoplasmas). Russian J Genetics 2001; 37: 979-92.

  58. Rottem S, Naot Y. Subversion and explotation of host cells by mycoplasmas. Trends Microbiol 1998; 6: 436-40.

  59. Rottem S. Interaction of mycoplasmas with host cells. Physiol Rev 2003; 83: 417-32.

  60. Gallegos-Ávila G, Ortega-Martínez M, Ramos-González B, Tijerina-Menchaca R, Ancer-Rodríguez J, Jaramillo-Rangel G. Ultrastructural findings in semen samples of infertile men infected with Chlamydia trachomatis and mycoplasmas. Fertil Steril 2009; 91: 915-19.

  61. Reichart M, Kahane I, Bartoov B. In vivo and in vitro impairment of human and ram sperm nuclear chromatin integrity by sexually transmitted Ureaplasma urealyticum infection. Biol Reprod 2000; 63: 1041-48.

  62. Christiansen G, Birkelund S. Transmission electron microscopy and immunogold staining of mollicute surface antigens. Methods Mol Biol 1998; 104: 309-18.

  63. Díaz-García FJ. Interacción de Mycoplasma hominis y Ureaplasma urealyticum con espermatozoides humanos. Modelo in vitro [tesis doctoral]. México: Escuela Nacional de Ciencias Biológicas, IPN; 2007.

  64. Lingwood CA. Colocalization of sulfogalactosylacylalkylglicerol (SGG) and its binding protein during spermatogenesis and sperm maturation. Topology of SGG defines a new testicular germ cell membrane domain. Biochem Cell Biol 1986; 64: 984-93.

  65. Vos JP, Lopes-Cardozo M, Gazella BM. Metabolic and functional aspects of sulfogalactolipids. Biochim Biophys Acta 1994; 1211: 125-49.

  66. Lingwood C, Shramayr S, Quinn P. Male germ cell specific sulfogalacto-glycerolipid is recognized and degraded by mycoplasmas associated with male infertility. J Cell Physiol 1990; 142: 170-76.

  67. Lingwood CA, Quinn PA, Wilansky S. Common sulfoglycolipid receptor for mycoplasmas involved in animal and human infertility. Biol Reprod 1990: 43, 694-97.

  68. Henrich B, Feldmann R, Hadding U. Cytoadhesins of Mycoplasma hominis. Infect Immun 1993; 61: 2945-51.

  69. Olson LD, Gilbert AA. Characteristics of Mycoplasma hominis adhesion. J Bacteriol 1993; 175: 3224-27.

  70. Boulanger J, Faulds D, Eddy EM, Lingwood CA. Members of the 70 kDa heat shock protein family specifically recognize sulfoglycolipids: Role in gamete recognition and mycoplasma-related infertility. J Cell Physiol 1995; 165: 7-17.

  71. Garcia-Romero CS. Detección y caracterización parcial de las proteínas mediadoras de adherencia a Mycoplasma hominis y Ureaplasma urealyticum en espermatozoides humanos. [tesis de licenciatura]. México: Escuela Nacional de Ciencias Biológicas, IPN; 2006.

  72. Aitken RJ, Baker MA. Oxidative stress and reproductive biology. Reprod Fertil Develop 2004; 16: 581-88.

  73. Potts JM, Sharma R, Pasqualotto F, Nelson D, Hall G, Agarwal A. Association of Ureaplasma urealyticum with abnormal reactive oxygen species levels and absence of leukocytospermia. J Urol 2000; 163: 1775-78.

  74. Avron A, Gallily R. Mycoplasma stimulates the production of oxidative radicals by murine peritoneal macrophages. J Leukocyte Biol 1995; 57: 264-68.

  75. Miller RA, Britigan BE. Role of oxidants in microbial pathophysiology. Clin Microbiol Rev 1997; 10: 1-18.

  76. Talkington DF, Davis JK, Canupp KC, Garret BK, Waites KB, Huster GA et al. The effects of three serotypes of Ureaplasma urealyticum on spermatozoal motility and penetration in vitro. Fertil Steril 1991; 55: 170-76.

  77. Reichart M, Levi H, Kahane I, Bartoov B. Dual energy metabolism-dependent effect of Ureaplasma urealyticum infection on sperm activity. J Androl 2001; 22: 404-11.

  78. Waites KB, Katz B, Schelonka RI. Mycoplasmas and ureaplasmas as neonatal pathogens. Clin Microbiol Rev 2005; 18: 757-89.

  79. Pollack DJ, Williams MV, McElhaney RN. The comparative metabolism of the Mollicutes (Mycoplasmas): The utility for taxonomic classification and the relationship of putative gene annotation and phylogeny to enzymatic function in the smallest free-living cells. Crit Rev Microbiol 1997; 23: 269-354.

  80. Rawadi G, Roman S. Mycoplasma membrane lipoproteins induce proinflammatory cytokines by a mechanism distinct from that of lipopolysaccharide. Infect Immun 1996; 64: 637-43.

  81. Salman M, Rottem S. The cell membrane of Mycoplasma penetrans: lipid composition and phospholipase A1 activity. Biochim Biophys Acta 1995; 1235: 369-77.

  82. Shibata KI, Sasaki T, Watanabe T. AIDS-associated mycoplasmas possess phospholipases C in the membrane. Infect Immun 1995; 63: 4174-77.

  83. Salman M, Borovsky Z, Rottem S. Mycoplasma penetrans infection of MOLT-3 lymphocytes induces changes in the lipid composition of host cells. Microbiology 1998; 144: 3447-54.

  84. Bendjennat M, Blanchard A, Loutfi M, Montagnier L, Bahraoui E. Purification and characterization of Mycoplasma penetrans Ca2+/Mg2+ -dependent endonuclease. J Bacteriol 1997; 179: 2210-20.

  85. Bendjennat M, Blanchard A, Loutfi M, Montagnier L, Bahraoui E. Role of Mycoplasma penetrans endonuclease P40 as a potential pathogenic determinant. Infect Immun 1999; 6: 4456-62.

  86. Berg TG, Philpot KL, Welsh MS, Sanger WG, Smith CV. Ureaplasma/ Mycoplasma -infected amniotic fluid: pregnancy outcome in treated and nontreated patients. J Perinatol 1999; 19: 275-77.

  87. Gallegos G, Ramos B, Santiso R, Goyanes V, Gosálvez J, Fernandez JL. Sperm DNA fragmentation in infertile men with genitourinary infection by Chlamydia trachomatis and mycoplasmas. Fertil Steril 2008; 90: 328-34.

  88. Kanakas N, Mantzavinos T, Boufidou F, Koumentakou I, Creatsas G. Ureaplasma urealyticum in semen: is there any effect on in vitro fertilization outcome? Fertil Steril 1999; 71: 523-27.

  89. Paddenberg R, Wulf S, Weber A, Heimann P, Beck LA, Mannherz HG. Internucleosomal DNA fragmentation in cultured cells under conditions reported to induce apoptosis may be caused by mycoplasma endonucleases. Eur J Cell Biol 1996; 69: 105-19.

  90. Tsai S, Wear JD, Shih JW, Lo SC. Mycoplasmas and oncogenesis: persistent infection and multistage malignant transformation. Proc Natl Acad Sci USA 1995; 92: 10197-201.

  91. Law H, Itkonnen O, Lingwood CA. The sulfogalactolipid binding protein SLIP 1: a conserved function for a conserved protein. J Cell Physiol 1988; 137: 462-68.

  92. Weerachatyanukul W, Rattanachaiyanont M, Carmona E, Furimsky A, Mai A et al. Sulfogalactosylglycerolipid in involved in human gamete interaction. Mol Reprod Develop 2001; 60: 569-78.

  93. Spehr M, Gisselmann G, Poplawski A, Riffell JA, Wetzel CH, Zimmer RK et al. Identification of testicular odorant receptor mediating human sperm chemotaxis. Science 2003; 299: 2054-58.

  94. Spehr M, Schwane K, Riffell JA, Zimmer RK, Hatt H. Odorant receptors and olfactory-like signaling mechanisms in mammalian sperm. Mol Cell Endocrinol 2006; 250: 128-36.

  95. Miraglia E, Rullo ML, Bosia A, Massobrio M, Revellz A, Ghigo D. Stimulation of the nitric oxide/cyclic guanosine monophosphate signaling pathway elicits human sperm chemotaxis in vitro. Fertil Steril 2007; 87: 1059-63.

  96. Baldi E, Luconi M, Bonaccorsi L, Krausz C, Forti G. Human sperm activation during capacitation and acrosome reaction: role of calcium, protein phosphorylation and lipid remodelling pathways. Front Biosci 1996; 1: d189-205.

  97. Knobil E, Nelly J, Ewing L, Greenwald G, Markert C, Pfaff D. The Physiology of Reproduction. New York: Raven Press; 1988.

  98. Cole BC. Mycoplasma interactions with the immune system: implications for disease pathology. ASM News 1996; 62: 471-75.

  99. Shi J, Yang Z, Wang M, Cheng G, Li D, Wang Y et al. Screening of an antigen target for immunocontraceptives from cross-reactive antigens between human sperm and Ureaplasma urealyticum. Infect Immun 2007; 75: 2004-11.

  100. Turek PJ. Infections, immunology and male infertility. Infertil Rep Med Clin North Am 1999; 10: 435-68.

  101. Pannekoek Y, Trum JW, Bleker OP, van-der-Veen F, Spanjaard L, Dankert J. Cytokine concentrations in seminal plasma from subfertile men are not inicative of the presence of Ureaplasma urealyticum or Mycoplasma hominis in the lower genital tract. J Med Microbiol 2000; 49: 697-700.

  102. Zhang S, Wear DJ, Lo SC. Mycoplasmal infections alter gene expression in cultured human prostatic and cervical epithelial cell. FEMS Immunol Med Microbiol 2000; 27: 43-50.

  103. Casadevall A, Pirofski LA. Host-pathogen interactions: redefining the basic concepts of virulence and pathogenicity. Infect Immun 1999; 67: 3703-13.

  104. Jeremias J, Giraldo P, Durrant S, Ribeiro-Filho A, Witkin SS. Relationship between Ureaplasma urealyticum vaginal colonization and polymorphism in the interleukin-1 receptor antagonist gene. J Infect Dis 1999; 180: 912-14.

  105. Kwiatkowski D. Science, medicine, and the future: Susceptibility to infection. Brit Med J 2000; 321: 1061-65.

  106. Burrack LS, Higgin DE. Genomic approaches to understanding bacterial virulence. Curr Op Microbiol 2007; 10: 4-9.

  107. Jaffe JD, Berg HC, Church GM. Proteogenomic mapping as a complementary method to perform genome annotation. Proteomics 2004; 4: 5-77.

  108. Fraser CM, Gocayne JD, White O, Adams MD, Clayton RA, Fleischmann RD et al. The minimal gene complement of Mycoplasma genitalium. Science 1995; 270: 397-404.

  109. Glass JI, Lefkowitz EJ, Glass JS, Heiner CR, Chen EY, Cassell GH. The complete sequence of the mucosal pathogen Ureaplasma urealyticum. Nature 2000; 407: 757-62.

  110. Pereyre S, Sirand-Pugnet P, Charron A, Renaudin H, Barré A, Avenaud P et al. Life on arginine for Mycoplasma hominis: Clues from its minimal genome and comparison with other human urogenital mycoplasmas. PLoS Genetics 2009; 5: e1000677.

  111. Pinto PM, Chemale G, Amara-de-Castro L, Metz-Costa AP, Deon-Kich J; Henning-Vainstein et al. Proteomic survey of the pathogenic Mycoplasma hyopneumoniae strain 7448 and identification of novel post-translationally modified and antigenic proteins. Vet Microbiol 2007; 121: 83-93.

  112. Regula JT, Ueberle B, Boguth G, Görg A, Schnölzer M, Herrmann R et al. Towards a two-dimensional proteome map of Mycoplasma pneumoniae. Electrophoresis 2000; 21: 3765-80.

  113. Ferrer-Navarro M, Gómez A, Yanes O, Planell R, Avilés FX, Piñol J et al. Proteome of the bacterium Mycoplasma penetrans. J Proteome Res 2006; 5: 688-94.

  114. Liu YC, Lin IH, Chung WJ, Hu WS, Ng WV, Lu CH et al. Proteomics characterization of cytoplasmic and lipid-associated membrane proteins of human pathogen Mycoplasma fermentans M64. PLoS ONE 2012; 7: e35304. doi:10.1371/journal.pone.0035304




2020     |     www.medigraphic.com