1,052
Views
42
CrossRef citations to date
0
Altmetric
Original Article

A role for CXCL13 (BCA-1) in pregnancy and intra-amniotic infection/inflammation

, MD, , MD, , , , , , , , , , , , & show all
Pages 763-775 | Received 21 Mar 2008, Accepted 30 May 2008, Published online: 07 Jul 2009

References

  • Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol 1988; 31: 553–584
  • Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, Sabo V, Athanassiadis A P, Hobbins J C. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol 1989; 161: 817–824
  • Romero R, Mazor M, Munoz H, Gomez R, Galasso M, Sherer D M. The preterm labor syndrome. Ann N Y Acad Sci 1994; 734: 414–429
  • Goncalves L F, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 2002; 8: 3–13
  • Romero R, Espinoza J, Kusanovic J P, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG 2006; 113(Suppl 3)17–42
  • MacDorman M F, Hoyert D L, Martin J A, Munson M L, Hamilton B E. Fetal and perinatal mortality, United States, 2003. Natl Vital Stat Rep 2007; 55: 1–17
  • Romero R, Gomez R, Araneda H, Ramirez M, Cotton D B. Cervical mucus inhibits microbial growth: A host defense mechanism to prevent ascending infection in pregnant and non-pregnant women. American Journal of Obestrics and Gynecology 1993; 168: A57
  • Svinarich D M, Wolf N A, Gomez R, Gonik B, Romero R. Detection of human defensin 5 in reproductive tissues. Am J Obstet Gynecol 1997; 176: 470–475
  • Eggert-Kruse W, Botz I, Pohl S, Rohr G, Strowitzki T. Antimicrobial activity of human cervical mucus. Hum Reprod 2000; 15: 778–784
  • Hein M, Valore E V, Helmig R B, Uldbjerg N, Ganz T. Antimicrobial factors in the cervical mucus plug. Am J Obstet Gynecol 2002; 187: 137–144
  • Hein M, Helmig R B, Schonheyder H C, Ganz T, Uldbjerg N. An in vitro study of antibacterial properties of the cervical mucus plug in pregnancy. Am J Obstet Gynecol 2001; 185: 586–592
  • Svinarich D M, Gomez R, Romero R. Detection of human defensins in the placenta. Am J Reprod Immunol 1997; 38: 252–255
  • Talmi Y P, Sigler L, Inge E, Finkelstein Y, Zohar Y. Antibacterial properties of human amniotic membranes. Placenta 1991; 12: 285–288
  • Kjaergaard N, Hein M, Hyttel L, Helmig R B, Schonheyder H C, Uldbjerg N, Madsen H. Antibacterial properties of human amnion and chorion in vitro. Eur J Obstet Gynecol Reprod Biol 2001; 94: 224–229
  • Guleria I, Pollard J W. The trophoblast is a component of the innate immune system during pregnancy. Nat Med 2000; 6: 589–593
  • Espinoza J, Chaiworapongsa T, Romero R, Edwin S, Rathnasabapathy C, Gomez R, Bujold E, Camacho N, Kim Y M, Hassan S, et al. Antimicrobial peptides in amniotic fluid: Defensins, calprotectin and bacterial/permeability-increasing protein in patients with microbial invasion of the amniotic cavity, intra-amniotic inflammation, preterm labor and premature rupture of membranes. J Matern Fetal Neonatal Med 2003; 13: 2–21
  • Esplin M S, Romero R, Chaiworapongsa T, Kim Y M, Edwin S, Gomez R, Mazor M, Adashi E Y. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J Matern Fetal Neonatal Med 2005; 17: 365–373
  • Suzuki Y, Yamamoto T, Kojima K, Tanemura M, Tateyama H, Suzumori K. Evaluation levels of cytokines in amniotic fluid of women with intrauterine infection in the early second trimester. Fetal Diagn Ther 2006; 21: 45–50
  • Soto E, Espinoza J, Nien J K, Kusanovic J P, Erez O, Richani K, Santolaya-Forgas J, Romero R. Human beta-defensin-2: A natural antimicrobial peptide present in amniotic fluid participates in the host response to microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 2007; 20: 15–22
  • Zlotnik A, Yoshie O. Chemokines: A new classification system and their role in immunity. Immunity 2000; 12: 121–127
  • Athayde N, Romero R, Maymon E, Gomez R, Pacora P, Araneda H, Yoon B H. A role for the novel cytokine RANTES in pregnancy and parturition. Am J Obstet Gynecol 1999; 181: 989–994
  • Cohen J, Ghezzi F, Romero R, Ghidini A, Mazor M, Tolosa J E, Goncalves L F, Gomez R. GRO alpha in the fetomaternal and amniotic fluid compartments during pregnancy and parturition. Am J Reprod Immunol 1996; 35: 23–29
  • Romero R, Ceska M, Avila C, Mazor M, Behnke E, Lindley I. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am J Obstet Gynecol 1991; 165(4 Pt 1)813–820
  • Shimoya K, Zhang Q, Tenma K, Ota Y, Hashimoto K, Shizusawa Y, Kimura T, Koyama M, Murata Y. Fractalkine (FRK) levels in amniotic fluid and its production during pregnancy. Mol Hum Reprod 2003; 9: 97–101
  • Keelan J A, Yang J, Romero R J, Chaiworapongsa T, Marvin K W, Sato T A, Mitchell M D. Epithelial cell-derived neutrophil-activating peptide-78 is present in fetal membranes and amniotic fluid at increased concentrations with intra-amniotic infection and preterm delivery. Biol Reprod 2004; 70: 253–259
  • Jacobsson B, Holst R M, Andersson B, Hagberg H. Monocyte chemotactic protein-2 and -3 in amniotic fluid: Relationship to microbial invasion of the amniotic cavity, intra-amniotic inflammation and preterm delivery. Acta Obstet Gynecol Scand 2005; 84: 566–571
  • Malamitsi-Puchner A, Vrachnis N, Samoli E, Baka S, Iliodromiti Z, Puchner K P, Malligianis P, Hassiakos D. Possible early prediction of preterm birth by determination of novel proinflammatory factors in midtrimester amniotic fluid. Ann N Y Acad Sci 2006; 1092: 440–449
  • Mittal P, Romero R, Kusanovic J P, Gotsch F, Mazaki-Tovi S, Espinoza J, Erez O, Nhan-Chang C L, Than N G, Vaisbuch E, et al. Granulocyte chemotactic protein-2 (CXCL6): A novel chemokine involved in the innate immune response of the amniotic cavity. Am J Obstet Gynecol 2007; 197: S68
  • Hamill N, Romero R, Gotsch F, Kusanovic J P, Edwin S, Erez O, Than N G, Mittal P, Espinoza J, Friel L, et al. Exodus 1 (CCL20): Evidence for the participation of this chemokine in spontaneous labor at term, preterm labor and intrauterine infection. J Perinat Med 2008; 36(3)217–227
  • Gunn M D, Ngo V N, Ansel K M, Ekland E H, Cyster J G, Williams L T. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 1998; 391: 799–803
  • Legler D F, Loetscher M, Roos R S, Clark-Lewis I, Baggiolini M, Moser B. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J Exp Med 1998; 187: 655–660
  • Vissers J L, Hartgers F C, Lindhout E, Figdor C G, Adema G J. BLC (CXCL13) is expressed by different dendritic cell subsets in vitro and in vivo. Eur J Immunol 2001; 31: 1544–1549
  • Widney D P, Breen E C, Boscardin W J, Kitchen S G, Alcantar J M, Smith J B, Zack J A, Detels R, Martinez-Maza O. Serum levels of the homeostatic B cell chemokine, CXCL13, are elevated during HIV infection. J Interferon Cytokine Res 2005; 25: 702–706
  • Carlsen H S, Baekkevold E S, Morton H C, Haraldsen G, Brandtzaeg P. Monocyte-like and mature macrophages produce CXCL13 (B cell-attracting chemokine 1) in inflammatory lesions with lymphoid neogenesis. Blood 2004; 104: 3021–3027
  • Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M, Forster R. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 2000; 192: 1545–1552
  • Cyster J G, Ansel K M, Reif K, Ekland E H, Hyman P L, Tang H L, Luther S A, Ngo V N. Follicular stromal cells and lymphocyte homing to follicles. Immunol Rev 2000; 176: 181–193
  • Wolniak K L, Shinall S M, Waldschmidt T J. The germinal center response. Crit Rev Immunol 2004; 24: 39–65
  • Muehlenbachs A, Fried M, Lachowitzer J, Mutabingwa T K, Duffy P E. Genome-wide expression analysis of placental malaria reveals features of lymphoid neogenesis during chronic infection. J Immunol 2007; 179: 557–565
  • Alexander G R, Himes J H, Kaufman R B, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996; 87: 163–168
  • Gonzalez R P, Gomez R M, Castro R S, Nien J K, Merino P O, Etchegaray A B, Carstens M R, Medina L H, Viviani P G, Rojas I T. [A national birth weight distribution curve according to gestational age in Chile from 1993 to 2000]. Rev Med Chile 2004; 132: 1155–1165
  • Yoon B H, Romero R, Moon J B, Shim S S, Kim M, Kim G, Jun J K. Clinical significance of intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2001; 185: 1130–1136
  • Romero R, Emamian M, Quintero R, Wan M, Hobbins J C, Mazor M, Edberg S. The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am J Obstet Gynecol 1988; 159: 114–119
  • Romero R, Jimenez C, Lohda A K, Nores J, Hanaoka S, Avila C, Callahan R, Mazor M, Hobbins J C, Diamond M P. Amniotic fluid glucose concentration: A rapid and simple method for the detection of intraamniotic infection in preterm labor. Am J Obstet Gynecol 1990; 163: 968–974
  • Romero R, Quintero R, Nores J, Avila C, Mazor M, Hanaoka S, Hagay Z, Merchant L, Hobbins J C. Amniotic fluid white blood cell count: A rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am J Obstet Gynecol 1991; 165(4 Pt 1)821–830
  • Romero R, Yoon B H, Mazor M, Gomez R, Diamond M P, Kenney J S, Ramirez M, Fidel P L, Sorokin Y, Cotton D. The diagnostic and prognostic value of amniotic fluid white blood cell count, glucose, interleukin-6, and Gram stain in patients with preterm labor and intact membranes. Am J Obstet Gynecol 1993; 169: 805–816
  • Kunkel S L. Through the looking glass: The diverse in vivo activities of chemokines. J Clin Invest 1999; 104: 1333–1334
  • Yoshie O, Imai T, Nomiyama H. Chemokines in immunity. Adv Immunol 2001; 78: 57–110
  • Zlotnik A, Yoshie O, Nomiyama H. The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol 2006; 7: 243
  • Muller G, Hopken U E, Lipp M. The impact of CCR7 and CXCR5 on lymphoid organ development and systemic immunity. Immunol Rev 2003; 195: 117–135
  • Schaerli P, Willimann K, Lang A B, Lipp M, Loetscher P, Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med 2000; 192: 1553–1562
  • Howard O M, Dong H F, Su S B, Caspi R R, Chen X, Plotz P, Oppenheim J J. Autoantigens signal through chemokine receptors: Uveitis antigens induce C. Blood 2005; 105: 4207–4214
  • Ebisuno Y, Tanaka T, Kanemitsu N, Kanda H, Yamaguchi K, Kaisho T, Akira S, Miyasaka M. Cutting edge: The B cell chemokine CXC chemokine ligand 13/B lymphocyte chemoattractant is expressed in the high endothelial venules of lymph nodes and Peyer's patches and affects B cell trafficking across high endothelial venules. J Immunol 2003; 171: 1642–1646
  • Rangel-Moreno J, Moyron-Quiroz J E, Hartson L, Kusser K, Randall T D. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. Proc Natl Acad Sci U S A 2007; 104: 10 577–10 582
  • Kanemitsu N, Ebisuno Y, Tanaka T, Otani K, Hayasaka H, Kaisho T, Akira S, Katagiri K, Kinashi T, Fujita N, et al. CXCL13 is an arrest chemokine for B cells in high endothelial venules. Blood 2005; 106: 2613–2618
  • Ansel K M, Ngo V N, Hyman P L, Luther S A, Forster R, Sedgwick J D, Browning J L, Lipp M, Cyster J G. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 2000; 406: 309–314
  • Ansel K M, Harris R B, Cyster J G. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002; 16: 67–76
  • Rangel-Moreno J, Moyron-Quiroz J, Kusser K, Hartson L, Nakano H, Randall T D. Role of CXC chemokine ligand 13, CC chemokine ligand (CCL) 19, and CCL21 in the organization and function of nasal-associated lymphoid tissue. J Immunol 2005; 175: 4904–4913
  • Arnold C N, Campbell D J, Lipp M, Butcher E C. The germinal center response is impaired in the absence of T cell-expressed CXCR5. Eur J Immunol 2007; 37: 100–109
  • Romagnani P, Lasagni L, Annunziato F, Serio M, Romagnani S. CXC chemokines: The regulatory link between inflammation and angiogenesis. Trends Immunol 2004; 25: 201–209
  • Spinetti G, Camarda G, Bernardini G, Romano D P, Capogrossi M C, Napolitano M. The chemokine CXCL13 (BCA-1) inhibits FGF-2 effects on endothelial cells. Biochem Biophys Res Commun 2001; 289: 19–24
  • Vermi W, Facchetti F, Riboldi E, Heine H, Scutera S, Stornello S, Ravarino D, Cappello P, Giovarelli M, Badolato R, et al. Role of dendritic cell-derived CXCL13 in the pathogenesis of Bartonella henselae B-rich granuloma. Blood 2006; 107: 454–462
  • Narayan K, Dail D, Li L, Cadavid D, Amrute S, Fitzgerald-Bocarsly P, Pachner A R. The nervous system as ectopic germinal center: CXCL13 and IgG in Lyme neuroborreliosis. Ann Neurol 2005; 57: 813–823
  • Rupprecht T A, Pfister H W, Angele B, Kastenbauer S, Wilske B, Koedel U. The chemokine CXCL13 (BLC): A putative diagnostic marker for neuroborreliosis. Neurology 2005; 65: 448–450
  • Gelderblom H, Londono D, Bai Y, Cabral E S, Quandt J, Hornung R, Martin R, Marques A, Cadavid D. High production of CXCL13 in blood and brain during persistent infection with the relapsing fever spirochete Borrelia turicatae. J Neuropathol Exp Neurol 2007; 66: 208–217
  • Chong Y, Nabeshima S, Furusyo N, Murata M, Yamaji K, Hayashi J. Downregulation of CXCR5 in CD27-B cells of HIV-1 infected patients. J Med Virol 2004; 73: 362–367
  • Luther S A, Lopez T, Bai W, Hanahan D, Cyster J G. BLC expression in pancreatic islets causes B cell recruitment and lymphotoxin-dependent lymphoid neogenesis. Immunity 2000; 12: 471–481
  • Shi K, Hayashida K, Kaneko M, Hashimoto J, Tomita T, Lipsky P E, Yoshikawa H, Ochi T. Lymphoid chemokine B cell-attracting chemokine-1 (CXCL13) is expressed in germinal center of ectopic lymphoid follicles within the synovium of chronic arthritis patients. J Immunol 2001; 166: 650–655
  • Weyand C M, Goronzy J J. Ectopic germinal center formation in rheumatoid synovitis. Ann N Y Acad Sci 2003; 987: 140–149
  • Smith J R, Braziel R M, Paoletti S, Lipp M, Uguccioni M, Rosenbaum J T. Expression of B-cell-attracting chemokine 1 (CXCL13) by malignant lymphocytes and vascular endothelium in primary central nervous system lymphoma. Blood 2003; 101: 815–821
  • Ishikawa S, Sato T, Abe M, Nagai S, Onai N, Yoneyama H, Zhang Y, Suzuki T, Hashimoto S, Shirai T, et al. Aberrant high expression of B lymphocyte chemokine (BLC/CXCL13) by C11b + CD11c+ dendritic cells in murine lupus and preferential chemotaxis of B1 cells towards BLC. J Exp Med 2001; 193: 1393–1402
  • Salomonsson S, Larsson P, Tengner P, Mellquist E, Hjelmstrom P, Wahren-Herlenius M. Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjogren's syndrome. Scand J Immunol 2002; 55: 336–342
  • Salomonsson S, Jonsson M V, Skarstein K, Brokstad K A, Hjelmstrom P, Wahren-Herlenius M, Jonsson R. Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjogren's syndrome. Arthritis Rheum 2003; 48: 3187–3201
  • Maglione P J, Xu J, Chan J. B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J Immunol 2007; 178: 7222–7234
  • Atlas E, Novak S N, Duray P H, Steere A C. Lyme myositis: Muscle invasion by Borrelia burgdorferi. Ann Intern Med 1988; 109: 245–246
  • Museteanu C, Schaible U E, Stehle T, Kramer M D, Simon M M. Myositis in mice inoculated with Borrelia burgdorferi. Am J Pathol 1991; 139: 1267–1271
  • Pachner A R, Dail D, Narayan K, Dutta K, Cadavid D. Increased expression of B-lymphocyte chemoattractant, but not pro-inflammatory cytokines, in muscle tissue in rhesus chronic Lyme borreliosis. Cytokine 2002; 19: 297–307
  • Ordi J, Ismail M R, Ventura P J, Kahigwa E, Hirt R, Cardesa A, Alonso P L, Menendez C. Massive chronic intervillositis of the placenta associated with malaria infection. Am J Surg Pathol 1998; 22: 1006–1011
  • Baecher-Allan C, Hafler D A. Suppressor T cells in human diseases. J Exp Med 2004; 200: 273–276
  • Robinson D S, Larche M, Durham S R. Tregs and allergic disease. J Clin Invest 2004; 114: 1389–1397
  • Lechler R I, Garden O A, Turka L A. The complementary roles of deletion and regulation in transplantation tolerance. Nat Rev Immunol 2003; 3: 147–158
  • Heikkinen J, Mottonen M, Alanen A, Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol 2004; 136: 373–378
  • Saito S, Sasaki Y, Sakai M. CD4(+)CD25 high regulatory T cells in human pregnancy. J Reprod Immunol 2005; 65: 111–120
  • Zenclussen A C, Gerlof K, Zenclussen M L, Ritschel S, Zambon B A, Fest S, Hontsu S, Ueha S, Matsushima K, Leber J, et al. Regulatory T cells induce a privileged tolerant microenvironment at the fetal–maternal interface. Eur J Immunol 2006; 36: 82–94
  • Lee B P, Chen W, Shi H, Der S D, Forster R, Zhang L. CXCR5/CXCL13 interaction is important for double-negative regulatory T cell homing to cardiac allografts. J Immunol 2006; 176: 5276–5283
  • Steinmetz O M, Panzer U, Kneissler U, Harendza S, Lipp M, Helmchen U, Stahl R A. BCA-1/CXCL13 expression is associated with CXCR5-positive B-cell cluster formation in acute renal transplant rejection. Kidney Int 2005; 67: 1616–1621
  • Wehner J, Morrell C N, Reynolds T, Rodriguez E R, Baldwin WM I II. Antibody and complement in transplant vasculopathy. Circ Res 2007; 100: 191–203
  • Mazzucchelli L, Blaser A, Kappeler A, Scharli P, Laissue J A, Baggiolini M, Uguccioni M. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J Clin Invest 1999; 104: R49–54
  • Zhou J, Law H K, Cheung C Y, Ng I H, Peiris J S, Lau Y L. Differential expression of chemokines and their receptors in adult and neonatal macrophages infected with human or avian influenza viruses. J Infect Dis 2006; 194: 61–70
  • Suzuki Y, Yamamoto T, Kojima K, Tanemura M, Tateyama H, Suzumori K. Evaluation levels of cytokines in amniotic fluid of women with intrauterine infection in the early second trimester. Fetal Diagn Ther 2006; 21: 45–50
  • Athayde N, Romero R, Maymon E, Gomez R, Pacora P, Yoon B H, Edwin S S. Interleukin 16 in pregnancy, parturition, rupture of fetal membranes, and microbial invasion of the amniotic cavity. Am J Obstet Gynecol 2000; 182(1 Pt 1)135–141
  • Chaiworapongsa T, Romero R, Espinoza J, Kim Y M, Edwin S, Bujold E, Gomez R, Kuivaniemi H. Macrophage migration inhibitory factor in patients with preterm parturition and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 2005; 18: 405–416
  • Ishikawa S, Nagai S, Sato T, Akadegawa K, Yoneyama H, Zhang Y Y, Onai N, Matsushima K. Increased circulating CD11b + CD11c+ dendritic cells (DC) in aged BWF1 mice which can be matured by TNF-alpha into BLC/CXCL13-producing DC. Eur J Immunol 2002; 32: 1881–1887
  • Perrier P, Martinez F O, Locati M, Bianchi G, Nebuloni M, Vago G, Bazzoni F, Sozzani S, Allavena P, Mantovani A. Distinct transcriptional programs activated by interleukin-10 with or without lipopolysaccharide in dendritic cells: Induction of the B cell-activating chemokine, CXC chemokine ligand 13. J Immunol 2004; 172: 7031–7042
  • Gardner L, Moffett A. Dendritic cells in the human decidua. Biol Reprod 2003; 69: 1438–1446
  • Berry S M, Romero R, Gomez R, Puder K S, Ghezzi F, Cotton D B, Bianchi D W. Premature parturition is characterized by in utero activation of the fetal immune system. Am J Obstet Gynecol 1995; 173: 1315–1320
  • Yoon B H, Romero R, Park J S, Kim M, Oh S Y, Kim C J, Jun J K. The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis. Am J Obstet Gynecol 2000; 183: 1124–1129
  • Yoon B H, Romero R, Yang S H, Jun J K, Kim I O, Choi J H, Syn H C. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996; 174: 1433–1440
  • Yoon B H, Jun J K, Romero R, Park K H, Gomez R, Choi J H, Kim I O. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997; 177: 19–26
  • Yoon B H, Romero R, Kim K S, Park J S, Ki S H, Kim B I, Jun J K. A systemic fetal inflammatory response and the development of bronchopulmonary dysplasia. Am J Obstet Gynecol 1999; 181: 773–779
  • Chaiworapongsa T, Romero R, Kim J C, Kim Y M, Blackwell S C, Yoon B H, Gomez R. Evidence for fetal involvement in the pathologic process of clinical chorioamnionitis. Am J Obstet Gynecol 2002; 186: 1178–1182
  • Laham N, Brennecke S P, Bendtzen K, Rice G E. Differential release of interleukin-6 from human gestational tissues in association with labour and in vitro endotoxin treatment. J Endocrinol 1996; 149: 431–439
  • Keelan J A, Sato T, Mitchell M D. Interleukin (IL)- 6 and IL-8 production by human amnion: Regulation by cytokines, growth factors, glucocorticoids, phorbol esters, and bacterial lipopolysaccharide. Biol Reprod 1997; 57: 1438–1444
  • Keelan J A, Wang K, Chaiworapongsa T, Romero R, Mitchell M D, Sato T A, Brown D A, Fairlie W D, Breit S N. Macrophage inhibitory cytokine 1 in fetal membranes and amniotic fluid from pregnancies with and without preterm labour and premature rupture of membranes. Mol Hum Reprod 2003; 9: 535–540
  • Hillyer P, Mordelet E, Flynn G, Male D. Chemokines, chemokine receptors and adhesion molecules on different human endothelia: Discriminating the tissue-specific functions that affect leucocyte migration. Clin Exp Immunol 2003; 134: 431–441
  • Steiniger B, Ulfig N, Risse M, Barth P J. Fetal and early post-natal development of the human spleen: From primordial arterial B cell lobules to a non-segmented organ. Histochem Cell Biol 2007; 128: 205–215

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.