The X-files of inflammation: Cellular mosaicism of X-linked polymorphic genes and the female advantage in the host response to injury and infection

Shock

Volumn 27, Issue 6, 2007, Pages 597-604

  Spolarics, Zoltán ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Bruton kinase; G6PD; Infection; IRAK; Mosaicism; NEMO; NF B; Sepsis; Sex; SNP; X chromosome

Indexed keywords

DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR;

APOPTOSIS; CELL POPULATION; CHROMOSOME MOSAICISM; DNA POLYMORPHISM; GENE EXPRESSION; GENE FREQUENCY; GENETIC TRAIT; GLUCOSE METABOLISM; HERITABILITY; HETEROZYGOSITY; HUMAN; IMMUNE RESPONSE; INFLAMMATORY DISEASE; INNATE IMMUNITY; METABOLIC REGULATION; PHENOTYPIC PLASTICITY; PHENOTYPIC VARIATION; REVIEW; SEPTIC SHOCK; SEX DIFFERENCE; X CHROMOSOME; X CHROMOSOME INACTIVATION;

ANIMALS; CHROMOSOMES, HUMAN, X; FEMALE; GLUCOSEPHOSPHATE DEHYDROGENASE; HUMANS; I-KAPPA B KINASE; INFECTION; INFLAMMATION; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LINKAGE (GENETICS); MALE; MOSAICISM; NF-KAPPA B; POLYMORPHISM, GENETIC; PROTEIN-TYROSINE KINASES; WOUNDS AND INJURIES;

EID: 34249033728     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e31802e40bd     Document Type: Review

References (91)

1. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP, et al.: The DNA sequence of the human X chromosome. Nature 434:325-337, 2005.
2. Gunter C: Genome biology: she moves in mysterious ways. Nature 434:279-280, 2005.
3. Aspinall R: Longevity and the immune response. Biogerontology 1:273-278, 2000.
4. Bartke A: Minireview: role of the growth hormone/insulin-like growth factor system in mammalian aging. Endocrinology 146:3718-3723, 2005.
5. Vina J, Borras C, Gambini J, Sastre J, Pallardo FV: Why females live longer than males: control of longevity by sex hormones. Sci Aging Knowledge Environ e17:2005, 2005.
6. Liu PY, Death AK, Handelsman DJ: Androgens and cardiovascular disease. Endocr Rev 24:313-340, 2003.
7. Chen CC, Parker CR Jr: Adrenal androgens and the immune system. Semin Reprod Med 22:369-377, 2004.
8. Angele MK, Schwacha MG, Ayala A, Chaudry IH: Effect of gender and sex hormones on immune responses following shock. Shock 14:81-90, 2000.
9. Kovacs EJ, Messingham KA, Gregory MS: Estrogen regulation of immune responses after injury. Mol Cell Endocrinol 193:129-135, 2002.
10. Choudhry MA, Bland KI, Chaudry IH: Gender and susceptibility to sepsis following trauma. Endocr Metab Immune Disord Drug Targets 6:127-135, 2006.
11. George RL, McGwin G Jr, Windham ST, Melton SM, Metzger J, Chaudry IH, Rue LW III: Age-related gender differential in outcome after blunt or penetrating trauma. Shock 19:28-32, 2003.
12. Gannon CJ, Pasquale M, Tracy JK, McCarter RJ, Napolitano LM: Male gender is associated with increased risk for postinjury pneumonia. Shock 21:410-414, 2004.
13. Szalay L, Shimizu T, Suzuki T, Hsieh YC, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Androstenediol administration after trauma-hemorrhage attenuates inflammatory response, reduces organ damage, and improves survival following sepsis. Am J Physiol Gastrointest Liver Physiol 291:G260-G266, 2006.
14. Suzuki T, Shimizu T, Szalay L, Choudhry MA, Rue LW III, Bland KI, Chaudry IH: Androstenediol ameliorates alterations in immune cells cytokine production capacity in a two-hit model of trauma-hemorrhage and sepsis. Cytokine 34:76-84, 2006.
15. Hsieh YC, Yu HP, Suzuki T, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Upregulation of mitochondrial respiratory complex IV by estrogen receptor-beta is critical for inhibiting mitochondrial apoptotic signaling and restoring cardiac functions following trauma-hemorrhage. J Mol Cell Cardiol 41:511-521, 2006.
16. Yang S, Choudhry MA, Hsieh YC, Hu S, Rue LW III, Bland KI, Chaudry IH: Estrus cycle: influence on cardiac function following trauma-hemorrhage. Am J Physiol Heart Circ Physiol 291:H2807-H2815, 2006.
17. Deitch EA, Ananthakrishnan P, Cohen DB, Xu DZ, Feketeova E, Hauser CJ: Neutrophil activation is modulated by sex hormones after trauma-hemorrhagic shock and burn injuries. Am J Physiol Heart Circ Physiol 291:H1456-H1465, 2006.
18. Maggio M, Basaria S, Ceda GP, Ble A, Ling SM, Bandinelli S, Valenti G, Ferrucci L: The relationship between testosterone and molecular markers of inflammation in older men. J Endocrinol Invest 28:116-119, 2005.
19. Weitzmann MN, Pacifici R: Estrogen regulation of immune cell bone interactions. Ann N Y Acad Sci 1068:256-274, 2006.
20. Hirschhorn JN, Lohmueller K, Byrne E, Hirschhorn K: A comprehensive review of genetic association studies. Genet Med 4:45-61, 2002.
21. Clark MF, Baudouin SV: A systematic review of the quality of genetic association studies in human sepsis. Intensive Care Med 32:1706-1712, 2006.
22. Lohmueller KE, Pearce CL, Pike M, Lander ES, Hirschhorn JN: Meta-analysis of genetic association studies supports a contribution of common variants to susceptibility to common disease. Nat Genet 33:177-182, 2003.
23. Arcaroli J, Fessler MB, Abraham E: Genetic polymorphisms and sepsis. Shock 24:300-312, 2005.
24. Hildebrand F, Pape HC, Griensven M, Meier S, Hasenkamp S, Krettek C, Stuhrmann M: Genetic predisposition for a compromised immune system after multiple trauma. Shock 24:518-522, 2005.
25. Tabrizi AR, Zehnbauer BA, Freeman BD, Buchman TG: Genetic markers in sepsis. J Am Coll Surg 192:106-117, 2001.
26. Van Deventer SJH: Cytokine and cytokine receptor polymorphisms in infectious disease. Intensive Care Med 26:98-102, 2000.
27. Wunderink RG, Waterer GW: Genetics of sepsis and pneumonia. Curr Opin Crit Care 9:384-389, 2003.
28. Rivera-Chavez FA, Peters-Hybki DL, Barber RC, O'Keefe GE: Interleukin-6 promoter haplotypes and interleukin-6 cytokine responses. Shock 20:218-223, 2003.
29. Heard E, Disteche CM: Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20:1848-1867, 2006.
30. Goto T, Monk M: Regulation of X-chromosome inactivation in development in mice and humans. Microbiol Mol Biol Rev 62:362-378, 1998.
31. Latham KE: X chromosome imprinting and inactivation in preimplantation mammalian embryos. Trends Genet 21:120-127, 2005.
32. Guo SW, Thompson EA: Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361-372, 1992.
33. Carrel L, Willard HF: X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400-404, 2005.
34. Abkowitz JL, Taboada M, Shelton GH, Catlin SN, Guttorp P, Kiklevich JV: An X chromosome gene regulates hematopoietic stem cell kinetics. Proc Natl Acad Sci U S A 95:3862-3866, 1998.
35. Hatakeyama C, Anderson CL, Beever CL, Penaherrera MS, Brown CJ, Robinson WP: The dynamics of X-inactivation skewing as women age. Clin Genet 66:327-332, 2004.
36. Brown CJ: Skewed X-chromosome inactivation: cause or consequence? J Natl Cancer Inst 91:304-305, 1999.
37. Koker MY, Sanal O, de Boer M, Tezcan I, Metin A, Tan C, Ersoy F, Roos D: Skewing of X-chromosome inactivation in three generations of carriers with X-linked chronic granulomatous disease within one family. Eur J Clin Invest 36:257-264, 2006.
38. Parrish JE, Scheuerle AE, Lewis RA, Levy ML, Nelson DL: Selection against mutant alleles in blood leukocytes is a consistent feature in incontinentia pigmenti type 2. Hum Mol Genet 5:1777-1783, 1996.
39. Migeon BR, Axelman J, Jan DB, Valle D, Mitchell GA, Rosenbaum KN: Selection against lethal alleles in females heterozygous for incontinentia pigmenti. Am J Hum Genet 44:100-106, 1989.
40. Peng H, Lakhani R, Lee C, Zheng Q, Chaggar RK, Wright NA, Pan L, Isaacson PG: Clonality analysis of defined cell populations in paraffin-embedded tissue sections by RT-PCR amplification of X-linked G6PD gene. J Pathol 191:313-317, 2000.
41. Griffiths DF, Davies SJ, Williams D, Williams GT, Williams ED: Demonstration of somatic mutation and colonic crypt clonality by X-linked enzyme histochemistry. Nature 333:461-463, 1988.
42. Wilmanski J, Siddiqi M, Deitch EA, Spolarics Z: Augmented IL-10 production and redox-dependent signaling pathways in glucose-6-phosphate dehydrogenase-deficient mouse peritoneal macrophages. J Leukoc Biol 78:85-94, 2005.
43. Spolarics Z, Condon MR, Siddiqi M, Machiedo GW, Deitch EA: Red blood cell dysfunction in septic glucose-6-phosphate dehydrogenase-deficient mice. Am J Physiol Heart Circ Physiol 286:H2118-H2126, 2004.
44. O'Neill LA: How toll-like receptors signal: what we know and what we don't know. Curr Opin Immunol 18:3-9, 2006.
45. Lye E, Mirtsos C, Suzuki N, Suzuki S, Yeh WC: The role of interleukin 1 receptor-associated kinase-4 (IRAK-4) kinase activity in IRAK-4-mediated signaling. J Biol Chem 279:40653-40658, 2004.
46. Janssens S, Beyaert R: Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol Cell 11:293-302, 2003.
47. Hayden MS, Ghosh S: Signaling to NF-kappa B. Genes Dev 18:2195-2224, 2004.
48. Suzuki N, Suzuki S, Yeh WC: IRAK-4 as the central TIR signaling mediator in innate immunity. Trends Immunol 23:503-506, 2002.
49. Arcaroli J, Silva E, Maloney JP, He Q, Svetkauskaite D, Murphy JR, Abraham E: Variant IRAK-1 haplotype is associated with increased nuclear factor-kappa B activation and worse outcomes in sepsis. Am J Respir Crit Care Med 173:1335-1341, 2006.
50. Tato CM, Hunter CA: Host-pathogen interactions: subversion and utilization of the NF-kappa B pathway during infection. Infect Immun 70:3311-3317, 2002.
51. Bubici C, Papa S, Pham CG, Zazzeroni F, Franzoso G: NF-kappa B and JNK: an intricate affair. Cell Cycle 3:1524-1529, 2004.
52. Wu CJ, Conze DB, Li T, Srinivasula SM, Ashwell JD: NEMO is a sensor of Lys 63-linked polyubiquitination and functions in NF-kappa B activation. Nat Cell Biol 8:398-406, 2006.
53. Ea CK, Deng L, Xia ZP, Pineda G, Chen ZJ: Activation of IKK by TNF alpha requires site-specific ubiquitination of RIP1 and polyubiquitin binding by NEMO. Mol Cell 22:245-257, 2006.
54. Burns KA, Martinon F: Inflammatory diseases: is ubiquitinated NEMO at the hub? Curr Biol 14:R1040-R1042, 2004.
55. Bartek J, Lukas J: Cell biology. The stress of finding NEMO. Science 311:1110-1111, 2006.
56. Wuerzberger-Davis SM, Nakamura Y, Seufzer BJ, Miyamoto S: NF-kappa B activation by combinations of NEMO SUMOylation and ATM activation stresses in the absence of DNA damage. Oncogene 26:641-651, 2007.
57. Mabb AM, Wuerzberger-Davis SM, Miyamoto S: PIASy mediates NEMO sumoylation and NF-kappa B activation in response to genotoxic stress. Nat Cell Biol 8:986-993, 2006.
58. Smahi A, Courtois G, Vabres P, Yamaoka S, Heuertz S, Munnich A, Israel A, Heiss NS, Klauck SM, Kioschis P, et al.: Genomic rearrangement in NEMO impairs NF-kappa B activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium. Nature 405:466-472, 2000.
59. Uzel G: The range of defects associated with nuclear factor kappa B essential modulator. Curr Opin Allergy Clin Immunol 5:513-518, 2005.
60. Aradhya S, Woffendin H, Jakins T, Bardaro T, Esposito T, Smahi A, Shaw C, Levy M, Munnich A, D'Urso M, et al.: A recurrent deletion in the ubiquitously expressed NEMO (IKK-gamma) gene accounts for the vast majority of incontinentia pigmenti mutations. Hum Mol Genet 10:2171-2179, 2001.
61. Nelson DL: NEMO, NF kappa B signaling and incontinentia pigmenti. Curr Opin Genet Dev 16:282-288, 2006.
62. Puel A, Picard C, Ku CL, Smahi A, Casanova JL: Inherited disorders of NF-kappa B-mediated immunity in man. Curr Opin Immunol 16:34-41, 2004.
63. Ku CL, Picard C, Erdos M, Jeurissen A, Bustamante J, Puel A, von Bernuth H, Filipe-Santos O, Chang H, Lawrence T, et al.: IRAK4 and NEMO mutations in otherwise healthy children with recurrent invasive pneumococcal disease. J Med Genet 44:16-23, 2007.
64. Gray P, Dunne A, Brikos C, Jefferies CA, Doyle SL, O'Neill LA: MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J Biol Chem 281:10489-10495, 2006.
65. Jefferies CA, O'Neill LA: Bruton's tyrosine kinase (Btk) - the critical tyrosine kinase in LPS signalling? Immunol Lett 92:15-22, 2004.
66. Vihinen M, Kwan SP, Lester T, Ochs HD, Resnick I, Valiaho J, Conley ME, Smith CI: Mutations of the human BTK gene coding for Bruton tyrosine kinase in X-linked agammaglobulinemia. Hum Mutat 13:280-285, 1999.
67. Lindvall JM, Blomberg KE, Valiaho J, Vargas L, Heinonen JE, Berglof A, Mohamed AJ, Nore BF, Vihinen M, Smith CI: Bruton's tyrosine kinase: cell biology, sequence conservation, mutation spectrum, siRNA modifications, and expression profiling. Immunol Rev 203:200-215, 2005.
68. Lopez-Granados E, Perez DD, Ferreira CA, Fontan CG, Garcia Rodriguez MC: A genotype-phenotype correlation study in a group of 54 patients with X-linked agammaglobulinemia. J Allergy Clin Immunol 116:690-697, 2005.
69. Zangemeister-Wittke U, Simon HU: An IAP in action: the multiple roles of survivin in differentiation, immunity and malignancy. Cell Cycle 3:1121-1123, 2004.
70. Liston P, Fong WG, Korneluk RG: The inhibitors of apoptosis: there is more to life than Bcl2. Oncogene 22:8568-8580, 2003.
71. Bratton SB, Cohen GM: Death receptors leave a caspase footprint that Smacs of XIAP. Cell Death Differ 10:4-6, 2003.
72. Yin W, Cheepala S, Clifford JL: Identification of a novel splice variant of X-linked inhibitor of apoptosis-associated factor 1. Biochem Biophys Res Commun 339:1148-1154, 2006.
73. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, et al.: Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549-554, 2001.
74. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N, Kroemer G: Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 84:215-222, 2002.
75. Porter AG, Urbano AG: Does apoptosis-inducing factor (AIF) have both life and death functions in cells? Bioessays 28:834-843, 2006.
76. Stasia MJ, Bordigoni P, Floret D, Brion JP, Bost-Bru C, Michel G, Gatel P, Durant-Vital D, Voelckel MA, Li XJ, et al.: Characterization of six novel mutations in the CYBB gene leading to different sub-types of X-linked chronic granulomatous disease. Hum Genet 116:72-82, 2005.
77. Wolach B, Ash S, Gavrieli R, Stark B, Yaniv I, Roos D: Acute lymphoblastic leukemia in a patient with chronic granulomatous disease and a novel mutation in CYBB: first report. Am J Hematol 80:50-54, 2005.
78. Rump A, Rosen-Wolff A, Gahr M, Seidenberg J, Roos C, Walter L, Gunther V, Roesler J: A splice-supporting intronic mutation in the last bp position of a cryptic exon within intron 6 of the CYBB gene induces its incorporation into the mRNA causing chronic granulomatous disease (CGD). Gene 371:174-181, 2006.
79. von Goessel H, Hossle JP, Seger R, Gungor T: Characterization of 17 new cases of X-linked chronic granulomatous disease with seven novel mutations in the CYBB gene. Exp Hematol 34:528-535, 2006.
80. Spolarics Z: Endotoxemia, pentose cycle, and the oxidant/antioxidant balance in the hepatic sinusoid. J Leukoc Biol 63:534-541, 1998.
81. Luzzatto L, Mehta A: Glucose 6 phosphate dehydrogenase deficiency. In Scriver CR, Beaudet AL, Sly WS, Valle D (eds.): The Metabolic and Molecular Bases of Inherited Disease. New York, NY: McGraw Hill, pp 3367-3398, 1995.
82. Beutler E: G6PD: population genetics and clinical manifestations. Blood Rev 10:45-52, 1996.
83. Mordmuller B, Turrini F, Long H, Kremsner PG, Arese P: Neutrophils and monocytes from subjects with the Mediterranean G6PD variant: effect of Plasmodium falciparum hemozoin on G6PD activity, oxidative burst and cytokine production. Eur Cytokine Netw 9:239-245, 1998.
84. Spolarics Z, Siddiqi M, Siegel JH, Garcia ZC, Stein DS, Ong H, Livingston DH, Denny T, Deitch EA: Increased incidence of sepsis and altered monocyte functions in severely injured type A glucose-6-phosphate dehydrogenase-deficient African American trauma patients. Crit Care Med 29:728-736, 2001.
85. Wilmanski J, Villanueva E, Deitch EA, Spolarics Z: G6PD deficiency and the inflammatory response to endotoxin and polymicrobial sepsis. Crit Care Med 2007. In press.
86. Okar DA, Wu C, Lange AJ: Regulation of the regulatory enzyme, 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Adv Enzyme Regul 44:123-154, 2004.
87. Rider MH, Bertrand L, Vertommen D, Michels PA, Rousseau GG, Hue L: 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem J 381:561-579, 2004.
88. Patel MS, Korotchkina LG: Regulation of the pyruvate dehydrogenase complex. Biochem Soc Trans 34:217-222, 2006.
89. Sugden MC, Holness MJ: Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 284:E855-E862, 2003.
90. Schaffner SF: The X chromosome in population genetics. Nat Rev Genet 5:43-51, 2004.
91. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES: Positive natural selection in the human lineage. Science 312:1614-1620, 2006.