Chimerism a natural ability to tolerate kin, evolutionary traits connecting mammalian and protochordates

Invertebrate Survival Journal

Volumn 6, Issue 1, 2009, Pages S9-S20

  Voskoboynik, A ^b  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Chimerism; Fu HC; Immunologic tolerance; Mammalian pregnancy; Stem cells; Tunicate; Uterine NK

Indexed keywords

EID: 84921764983     PISSN: None     EISSN: 1824307X     Source Type: Journal    
DOI: None     Document Type: Review

References (155)

1. Adams KM, Nelson JL. Microchimerism: An investigative frontier in autoimmunity and transplantation. JAMA 291: 1127-1131, 2004.
2. Anderson D, Billingham RE, Lampkin GH, Medawar PB. The use of skin grafting to distinguish between monozygotic and dizygotic twins in cattle. Heredity 5: 379-397, 1951.
3. Andrassy J, Kusaka S, Jankowska-Gan E, Torrealba JR, Haynes LD, Marthaler BR, et al. Tolerance to noninherited maternal MHC antigens in mice. J. Immunol. 171: 5554-5561, 2003.
4. Ashkar AA, Croy BA. Functions of uterine natural killer cells are mediated by interferon gamma production during murine pregnancy. Semin. Immunol. 13: 235-241, 2001.
5. Azumi K, Takahashi H, Miki Y, Fujie M, Usami T, Ishikawa H, et al. Construction of a cDNA microarray derived from the ascidian ciona intestinalis. Zool. Sci. 20: 1223-1229, 2003.
6. Baker RR, Bellis MA. Human sperm competition: copulation, masturbation and infidelity. Chapman & Hall, London, 1995.
7. Ballarin L, Cima F, Sabbadin A. Morula cells and histocompatibility in the colonial ascidian Botryllus schlosseri. Zool. Sci. 12: 757-764, 1995.
8. Ballarin L, Cima F, Sabbadin A. Phenoloxidase and cytotoxicity in the compound ascidian Botryllus schlosseri. Dev. Comp. Immunol. 22: 479-492, 1998.
9. Ballarin L, Cima F, Floreani M, Sabbadin A. Oxidative stress induces cytotoxicity during rejection reaction in the compound ascidian Botryllus schlosseri. Comp. Biochem. Physiol. 133C: 411-418, 2002.
10. Bancroft FW. Variation and fusion of colonies in compound ascidians. Proc. Calif. Acad. Sci. 3: 137-186, 1903.
11. Bauer M, Orescovic I, Schoell WM, Bianchi DW, Pertl B. Detection of maternal DNA in umbilical cord plasma by fluorescent PCR amplification of short tandem repeat sequences. Ann. N. Y. Acad. Sci. 945: 161-163, 2001.
12. Ben-Shlomo R, Douek J, Rinkevich B. Heterozygote deficiency and chimerism in remote populations of a colonial ascidian from New Zealand. Mar. Ecol. Prog. Ser. 209: 109-117, 2001.
13. Ben-Shlomo R, Paz G, Rinkevich B. Postglacial-period and recent invasions shape the population genetics of botryllid ascidians along European Atlantic coasts. Ecosystems 9: 1118-1127, 2006.
14. Ben-Shlomo R, Motro U, Paz G, Rinkevich B. Pattern of settlement and natural chimerism in the colonial urochordate Botryllus schlosseri. Genetica 132: 51-58, 2008.
15. Bianchi DW, Zickwolf GK, Weil GJ, Sylvester S, DeMaria MA. Male fetal progenitor cells persist in maternal blood for as long as 27 years postpartum. Proc. Natl. Acad. Sci. USA 93: 705-708, 1996.
16. Bianchi DW, Williams JM, Sullivan LM, Hanson FW, Klinger KW, Shuber AP. PCR quantitation of fetal cells in maternal blood in normal and aneuploid pregnancies. Am. J. Hum. Genet. 61: 822-829, 1997.
17. Bianchi DW, Simpson JL, Jackson LG, Elias S, Holzgreve W, Evans MI, et al. Fetal gender and aneuploidy detection using fetal cells in maternal blood: Analysis of NIFTY I data. national institute of child health and development fetal cell isolation study. Prenat. Diagn. 22: 609-615, 2002.
18. Bianchi DW. Fetomaternal cell trafficking: a story that begins with prenatal diagnosis and may end with stem cell therapy. J. Pediatr. Surg. 42:12-18, 2007.
19. Billingham RE, Lampkin GH, Medawar PB, Williams HL. Tolerance to homografts, twin diagnosis and the freemartin condition in cattle. Heredity 6: 200-212, 1952.
20. Billingham RE, Brent L, Medawar PB. Actively acquired tolerance of foreign cells. Nature 172: 603-606, 1953.
21. Billingham RE, Brent L. Acquired tolerance of foreign cells in newborn animals. Proc. R. Soc. Lond. B Biol. Sci. 146: 78-90, 1956.
22. Bix M, Liao NS, Zijlstra M, Loring J, Jaenisch R, Raulet D. Rejection of class I MHC-deficient haemopoietic cells by irradiated MHC-matched mice. Nature 349: 329-331, 1991.
23. Borroni EM, Bonecchi R, Baracchi C, Savino B, Mantovani A, Locati M. Chemokine decoy receptors: new players in reproductive immunology. Immunol. Invest. 37: 483-497, 2008.
24. Boyd HC, Weissman IL, Saito Y. Morphologic and genetic verification that Monterey Botryllus and Woods Hole Botryllus are the same species. Biol. Bull. 178: 239-250, 1990.
25. Burighel P, Cloney RA. Urochordata: Ascidiacea. In: Harrison FW, Ruppert EE (eds), Microscopic anatomy of invertebrates, Wiley-Liss, Inc., NY, pp. 221-347, 1997.
26. Burnet FM. "Self-recognition" in colonial marine forms and flowering plants in relation to the evolution of immunity. Nature 232: 230-235, 1971.
27. Burnet FM. Multiple polymorphism in relation to histocompatibility antigens. Nature 245: 359-361, 1973.
28. Buss LW. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sc. i USA 79: 5337-5341, 1982.
29. Buss LW, Grosberg RK. Morphogenetic basis for phenotypic differences in Hydroid competitive behavior. Nature 343: 63-66, 1990.
30. Canestro C, Bassham S, Postlethwait JH. Evolution of the thyroid: Anterior-posterior reorganization of the Oikopleura endostyle revealed by Otx, Pax 2/5/8, and Hox1 expression. Dev Dyn doi:10. 1002/dvdy. 21525, 2008
31. Cao YA, Wagers AJ, Beilhack A, Dusich J, Bachmann MH, Negrin RS, et al. Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc. Natl. Acad. Sci. USA 101: 221-226, 2004.
32. Chadwick-Furman NE, Weissman IL. Life history plasticity in chimaeras of the colonial ascidian Botryllus schlosseri. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262: 157-162, 1995.
33. Cima F, Sabbadin A, Ballarin L. Cellular aspects of allorecognition in the compound ascidian Botryllus schlosseri. Dev. Comp. Immunol. 28: 881-889, 2004.
34. Cima F, Sabbadin A, Zaniolo G, Ballarin L (2006) Colony specificity and chemotaxis in the compound ascidian Botryllus schlosseri. Comp. Biochem. Physiol. 145A: 376-382, 2006.
35. Claas FH, Gijbels Y, van der Velden-de Munck J, van Rood JJ. Induction of B cell unresponsiveness to noninherited maternal HLA antigens during fetal life. Science 241: 1815-1817, 1988.
36. Claas FH, Gijbels Y, von Veen A, de Waal LP, D'Amaro J, Persijn GG, et al. Selection of cross-match negative HLA-A and/or -B mismatched donors for highly sensitized patients. Transplant. Proc. 21: 665-666, 1989.
37. Clark DA. Signaling at the fetomaternal interface. Am. J. Repros. Immunol. 41: 169-173, 1999.
38. De Tomaso AW, Nyholm SV, Palmeri KJ, Ishizuka KJ, Ludington WB, Mitchel K, et al. Isolation and characterization of a protochordate histocompatibility locus. Nature 438: 454-459, 2005.
39. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, et al. The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins. Science 298: 2157-2167, 2002.
40. Delsuc F, Brinkmann H, Chourrout D, Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrate. Nature 439: 965-968, 2006.
41. Dunn AD. Properties of an iodinating enzyme in the ascidian endostyle. Gen. Comp. Endocrinol. 40: 484-493, 1980.
42. Dunsford I, Bowley CC, Hutchison AM, Thompson JS, Sanger R, Race RR. A human blood-group chimera. Br. Med. J. 2: 80-81, 1953.
43. Emery D, McCullagh P. Immunological reactivity between chimeric cattle twins. I. homograft reaction. Transplantation 29: 4-9, 1980a.
44. Emery D, McCullagh P. Immunological reactivity between chimeric cattle twins. II. normal lymphocyte transfer. Transplantation 29: 10-16, 1980b.
45. Evans PC, Lambert N, Maloney S, Furst DE, Moore JM, Nelson JL. Long-term fetal microchimerism in peripheral blood mononuclear cell subsets in healthy women and women with scleroderma. Blood 93: 2033-2037, 1999.
46. Fagan MB, Weissman IL. HSP70 genes and historecognition in Botryllus schlosseri: Implications for MHC evolution. Hereditas 127: 25-35, 1997.
47. Gaillard MC, Ouvre E, Liegeois A, Lewin D. The concentration of fetal cells in maternal haematopoietic organs during pregnancy. an experimental study in mice (author's transl). J. Gynecol. Obstet. Biol. Reprod. (Paris) 7: 1043-1050, 1978.
48. Grosberg RK. Limited dispersal and proximity dependent mating success in Botryllus schlosseri. Evolution 41: 372-384, 1987.
49. Grosberg RK. The evolution of allorecognition specificity in colonial invertebrates. Quart. Rev. Biol. 63: 377-412, 1988.
50. Grosberg RK, Quinn JF. The genetic control and consequences of kin recognition by the larvae of a colonial marine invertebrate. Nature 322: 456-459, 1986.
51. Guleria I, Sayegh MH. Maternal acceptance of the fetus: true human tolerance. J. Immunol. 178: 3345-3351, 2007.
52. Hall JM, Lingenfelter P, Adams SL, Lasser D, Hansen JA, Bean MA. Detection of Maternal Cells in Human Umbilical Cord Blood using Fluorescence in Situ Hybridization. Blood 86: 2829-2832, 1995.
53. Hamada H, Arinami T, Kubo T, Hamaguchi H, Iwasaki H. Fetal nucleated cells in maternal peripheral blood: Frequency and relationship to gestational age. Hum. Genet. 91: 427-432, 1993.
54. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at human fetal-maternal interface. Nat. Med. 12: 1065-1074, 2006.
55. Herzenberg LA, Bianchi DW, Schroder J, Cann HM, Iverson GM. Fetal cells in the blood of pregnant women: Detection and enrichment by fluorescence-activated cell sorting. Proc. Natl. Acad. Sci. USA 76: 1453-1455, 1979.
56. Hill JA. Immunological contribution to recurrent pregnancy loss. Baillieres Clin. Obster. Gynaecol. 6: 489-438, 1992.
57. Hirose E, Saito Y, Watanabe H. Anew type of the manifestation of the colony specificity in the compound ascidian, Botrylloides violaceus Oka. Biol. Bull. 175: 240-245, 1988.
58. Hirose E, Saito Y, Watanabe H. Allogeneic rejection induced by the cut surface contact in the compound ascidian, Botrylloides simodensis. Invertebr. Dev. Reprod. 17: 159-164, 1990.
59. Hiruta J, Mazet F, Yasui K, Zhang P, Ogasawara M. Comparative expression analysis of transcription factor genes in the endostyle of invertebrate chordates. Dev. Dyn. 233: 1031-1037, 2005.
60. Höglund P, Ohlén C, Carbone E, Franksson L, Ljunggren HG, Latour A, et al. Recognition of beta-2microglobulin-negative (beta 2m-) T-cell blasts by natural killer cells from normal but not from beta 2m-mice: nonresponsiveness controlled by beta 2m-bone marrow ib chimeric mice. Proc. Natl. Acad. Sci. USA 88: 10332-10336, 1991.
61. Hunt JS, Petroff MG, McIntire RH Ober C. HLA-G and immune tolerance in pregnancy. FASEB J. 19: 682-693, 2005.
62. Ishitani A, Sageshima N, Lee N, Dorofeeva N, Hatake K, Marquardt H, et al. Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition. J. Immunol. 171: 1376-1384, 2003.
63. Kammerer U, Kruse A, Barrientos G, Arck PC, Blois SM. Role of dendritic cells in the regulation of maternal immune responses to the fetus during mammalian gestation. Immunol. Invest. 37: 499-533, 2008.
64. Kaplan J, Land S. Influence of maternal-fetal histocompatibility and MHC zygosity on maternal microchimerism. J. Immunol. 174: 7123-7128, 2005.
65. Karakashian S, Milkman R. Colony fusion compatibility types in Botryllus schlosseri. Biol. Bull. 133: 473-?, 1967.
66. Kaufman J. The origins of the adaptive immune system: Whatever next? Nat. Immunol. 3: 1124-1125, 2002.
67. Khalturin K, Becker M, Rinkevich B, Bosch TC. Urochordates and the origin of natural killer cells: Identification of a CD94/NKR-P1-related receptor in blood cells of Botryllus. Proc. Natl. Acad. Sci. USA 100: 622-627, 2003.
68. Khosrotehrani K, Johnson KL, Guegan S, Stroh H, Bianchi DW. Natural history of fetal cell microchimerism during and following murine pregnancy. J. Reprod. Immunol. 66: 1-12, 2005.
69. King A, Allan DS, Bowen M, Powis SJ, Joseph S, Verma S, et al. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30: 1623-1631, 2000.
70. Kitchens WH, Uehara S, Chase CM, Colvin RB, Russell PS, Madsen JC. The changing role of natural killer cells in solid organ rejection and tolerance. Transplantation 81: 811-817, 2006.
71. Klein J. Are invertebrates capable of anticipatory immune responses?. Scand. J. Immunol. 29: 499-505, 1989.
72. Koopmans M, Kremer Hovinga IC, Baelde HJ, Fernandes RJ, de Heer E, Bruijn JA, et al. Chimerism in kidneys, livers and hearts of normal women: Implications for transplantation studies. Am. J. Transplant. 5: 1495-1502, 2005.
73. Kurpisz M, Fernandez N, Fiszer D. The expression of MHC genes in reproductive organs and their role in reproduction. In: Kurspiz M, Fernandez N (eds), Immunology of human reproduction, Bios Scientific Publishers, Oxford, pp163-184, 1995.
74. Laird DJ, De Tomaso AW, Cooper MD, Weissman IL. 50 million years of chordate evolution: Seeking the origins of adaptive immunity. Proc. Natl. Acad. Sci. USA 97: 6924-6926, 2000.
75. Laird DJ, De Tomaso AW, Weissman IL. Stem cells are units of natural selection in a colonial ascidian. Cell 123: 1351-1360, 2005.
76. Liegeois A. In: Edelman P, Sureau C (eds) Immunologie de le reproduction humanie, Edition Boz., Paris, pp 99-100, 1983.
77. Lightner A, Schust DJ, Chen YBA, Barrier BF. The fetal allograft revisited: Does the study of an ancient invertebrate species shed light on the role of natural killer cells at the maternal-fetal interface? Clin. Dev. Immunol. 2008;2008:631920.
78. Lillie FR. The theory of the free-martin. Science 43: 611-613, 1916.
79. Litman GW, Cannon JP, Dishaw LJ. Reconstructing immune phylogeny: New perspectives. Nat. Rev. Immunol. 5: 866-879, 2005.
80. Litman GW, Dishaw LJ, Cannon JP, Haire RN, Rast JP. Alternative mechanisms of immune receptor diversity. Curr. Opin. Immunol. 19: 526-534, 2007.
81. Lo ES, Lo YM, Hjelm NM, Thilaganathan B. Transfer of nucleated maternal cells into fetal circulation during the second trimester of pregnancy. Br. J. Haematol. 100: 605-606, 1998.
82. Lo YM, Patel P, Wainscoat JS, Sampietro M, Gillmer MD, Fleming KA. Prenatal sex determination by DNA amplification from maternal peripheral blood. Lancet 2: 1363-1365, 1989.
83. Lo YM, Lo ES, Watson N, Noakes L, Sargent IL, Thilaganathan B, et al. Two-way cell traffic between mother and fetus: Biologic and clinical implications. Blood 88: 4390-4395, 1996.
84. Loubiere LS, Lambert NC, Flinn LJ, Erickson TD, Yan Z, Guthrie KA, et al. Maternal microchimerism in healthy adults in lymphocytes, monocyte/macrophages and NK cells. Lab. Invest. 86: 1185-1192, 2006.
85. Maloney S, Smith A, Furst DE, Myerson D, Rupert K, Evans PC, et al. Microchimerism of maternal origin persists into adult life. J. Clin. Invest. 104: 41-47, 1999.
86. Manastar I, Mandelboim O. The unique properties of human NK cells in the uterine mucosa. Placenta 22: S60-S66, 2008.
87. Manilay JO, Sykes M. Natural killer cells and their role in graft rejection Curr. Opin. Immunol. 10: 532-538, 1998.
88. Manni L, Burighel P. Common and divergent pathways in alternative developmental processes of ascians. BioEssays 28: 902-912, 2006.
89. Manni L, Zaniolo G, Cima F, Burighel P, Ballarin L. Botryllus schlosseri: a model ascidian for the study of asexual reproduction. Dev. Dyn. 236: 335-352, 2007.
90. Marleau AM, Greenwood JD, Wei Q, Singh B, Croy BA. Chimerism of murine fetal bone marrow by maternal cells occurs in late gestation and persists into adulthood. Lab. Invest. 83: 673-681, 2003.
91. Mold JE, Michaelsson J, Burt TD, Muench MO, Beckerman KP, Busch MP, et al. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322: 1562-1565, 2008.
92. Mukai H. Experimental alteration of fusibility in compound ascidians. Sci. Rep. Tokyo Kyoiku Daigaku 13B: 51-73, 1987.
93. Mukai H, Watanabe H. Distribution of fusion incompatibility types in natural populations of the compound ascidian Botryllus primigenus. Proc. Jpn. Acad. 51: 44-47, 1975.
94. Muller WE, Pancer Z, Rinkevich B. Molecular cloning and localization of a novel serine protease from the colonial tunicate Botryllus schlosseri. Mol. Mar. Biol. Biotechnol. 3: 70-77, 1994.
95. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-1193, 1998.
96. Nilsson O, Fredriksson G, Ofverholm T, Ericson LE. Electron-microscopic immunocytochemistry of 5-hydroxytryptamine in the ascidian endostyle. Cell Tissue Res. 253: 137-143, 1988.
97. Nyholm SV, Passegue E, Ludington WB, Voskoboynik A, Mitchel K, Weissman IL, et al. Fester, A candidate allorecognition receptor from a primitive chordate. Immunity 25: 163-173, 2006.
98. O'Donoghue K, Chan J, de la Fuente J, Kennea N, Sandison A, Anderson JR, et al. Microchimerism in female bone marrow and bone decades after fetal mesenchymal stem-cell trafficking in pregnancy. Lancet 364: 179-182, 2004a.
99. O'Donoghue K, Fisk NM. Fetal stem cells. Best. Pract. Res. Clin. Obstet. Gynaecol. 18: 853-875, 2004b.
100. Oka H, Watanabe H. Colony specificity in compound ascidians as tested by fusion experiments (a preliminary report). Proc. Jpn. Acad. 33: 657-659, 1957.
101. Oka H, Watanabe H. problems of colony specificity in compound ascidians. Bull. Mar. Biol. Stat. Asamushi. 10: 153-155, 1960.
102. Oka H, Watanabe H. Problems of colony specificity, with special reference to the fusibility of ascidians. Kagaku 37: 307-313, 1967.
103. Oosterwijk JC, Mesker WE, Ouwerkerk-van Velzen MC, Knepfle CF, Wiesmeijer KC, Beverstock GC, et al. Fetal cell detection in maternal blood: A study in 236 samples using erythroblast morphology, DAB and HbF staining, and FISH analysis. Cytometry 32: 178-185, 1998.
104. Owen RD. Immunogenetic consequences of vascular anastomoses between bovin twins. Science 102: 400-401, 1945.
105. Owen RD, Wood HR, Foord AG, Sturgeon P, Baldwin LG. Evidence for actively tolerance to Rh antigens. Proc. Natl. Acad. Sci. USA 40: 420-424, 1954.
106. Pancer Z, Gershon H, Rinkevich B. cDNA cloning of a putative protochordate FK506-binding protein. Biochem. Biophys. Res. Commun. 197: 973-977, 1993.
107. Pancer Z, Gershon H, Rinkevich B. coexistence and possible parasitism of somatic and germ cell lines in chimeras of the colonial urochordate Botryllus schlosseri. Biol. Bull. 189: 106-112, 1995.
108. Pancer Z, Cooper EL, Muller WE. A tunicate (Botryllus schlosseri) cDNA reveals similarity to vertebrate antigen receptors. Immunogenetics 45: 69-72, 1996a.
109. Pancer Z, Leuck J, Rinkevich B, Steffen R, Muller I, Muller WE. Molecular cloning and sequence analysis of two cDNAs coding for putative anionic trypsinogens from the colonial urochordate Botryllus schlosseri (ascidiacea). Mol. Mar. Biol. Biotechnol. 5: 326-333, 1996b.
110. Pancer Z, Scheffer U, Muller I, Muller WE. Cloning of sponge (Geodia cydonium) and tunicate (Botryllus schlosseri) proteasome subunit epsilon (PRCE): Implications about the vertebrate MHC-encoded homologue LMP7 (PRCC). Biochem. Biophys. Res. Commun. 228: 406-410, 1996c.
111. Pancer Z, Diehl-Seifert B, Rinkevich B, Muller WE. A novel tunicate (Botryllus schlosseri) putative C-type lectin features an immunoglobulin domain. DNA Cell Biol. 16: 801-806, 1997.
112. Paz G, Douek J, Mo CQ, Goren M, Rinkevich B. Genetic structure of Botryllus schlosseri (Tunicata) populations from the Mediterranean coast of Israel. Mar. Ecol. Prog. Ser. 250: 163-174, 2003.
113. Pennati R, Groppelli S, Sotgia C, Candiani S, Pestarino M, De Bernardi F. Serotonin localization in Phallusia mammillata larvae and effects of 5-HT antagonists during larval development. Develop. Growth Differ. 43: 647-656, 2001.
114. Petit T, Dommergues M, Socie G, Dumez Y, Gluckman E, Brison O. Detection of Maternal Cells in Human Fetal Blood during the Third Trimester of Pregnancy using Allele-Specific PCR Amplification. Br. J. Haematol. 98: 767-771, 1997.
115. Petit T, Gluckman E, Carosella E, Brossard Y, Brison O, Socie G. A highly sensitive polymerase chain reaction method reveals the ubiquitous presence of maternal cells in human umbilical cord blood. Exp. Hematol. 23: 1601-1605, 1995.
116. Pineda-Krch M, Lehtila K. Costs and benefits of genetic heterogeneity within organisms. J. Evol. Biol. 17: 1167-1177, 2004.
117. Rinkevich B. Immunological resorption in Botryllus schlosseri (Tunicata) chimeras is characterized by multilevel hierarchical organization of histocompatibility alleles. A speculative endeavor. Biol. Bull. 184: 342-345, 1993.
118. Rinkevich B. Primitive immune systems: are your ways my ways? Immunol. Rev. 198: 25-35, 2004a.
119. Rinkevich B. Will two walk together, except they have agreed? J. Evol. Biol. 17: 1167-1177, 2004b.
120. Rinkevich B. Rejection patterns in botryllid ascidian immunity: The first tier of allorecognition. Can. J. Zool. 83: 101-121, 2005.
121. Rinkevich B, Weissman IL. Chimeras in colonial invertebrates - a synergidtic symbiosis or somatic and germ cell parasitism. Symbiosis 4: 117-134, 1987.
122. Rinkevich B, Weissman IL. Allogeneic resorption in colonial protochordates: Consequences of nonself recognition. Dev. Comp. Immunol. 16: 275-286, 1992a.
123. Rinkevich B, Weissman IL. Incidents of rejection and indifference in Fu/HC incompatible protochordate colonies. J. Exp. Zool. 263: 105-111, 1992b.
124. Rinkevich B, Lilker-Levav T, Goren M. Allorecognition/Xenorecognition responses in Botrylloides subpopulations from the Mediterranean coast of Israel. J. Exp. Zool. 270: 302-313, 1994.
125. Rinkevich B, Porat R, Goren M. Allorecognition elements on Urochordate histocompatibility locus indicate unprecedented extensive polymorphism. Proc. Biol. Sci. 259: 319-324, 1995.
126. Rinkevich B, Tartakover S, Gershon H. Contribution of morula cells to allogeneic responses in the colonial urochordate Botryllus schlosseri. Mar. Biol. 131: 227-236, 1998.
127. Rosner A, Paz G, Rinkevich B. Divergent roles of the DEAD-box protein BS-PL10, the urochordate homologue of human DDX3 and DDX3Y proteins, in colony astogeny and ontogeny. Dev. Dyn. 235: 1508-1521, 2006.
128. Rosner A, Rabinowitz C, Moiseeva E, Voskoboynik A, Rinkevich B. BS-Cadherin in the colonial urochordate Botryllus schlosseri: One protein, many functions. Dev. Biol. 304: 687-700, 2007.
129. Sabbadin A. Le basi geneticha della capacita di fusion fra colonies in Botryllus schlosseri (Ascidiacea). Rend. Accad. Naz. Lincei Ser. 32: 1031-1035, 1962.
130. Sabbadin A, Zaniolo G. Sexual differentiation and germ cell transfer in the colonial ascidian Botryllus schlosseri. J. Exp. Zool. 207: 289-304, 1979.
131. Sabbadin A. Formal genetics of ascidians. Am. Zool. 22: 765-777, 1982.
132. Sabbadin A, Astorri C. Chimeras and histocompatibility in the colonial ascidian Botryllus schlosseri. Dev. Comp. Immunol. 12: 737-747, 1988.
133. Sabbadin A, Zaniolo G, Ballarin L. Genetic and cytological aspects of histocompatibility in ascidians. Boll. Zool. 59: 167-173, 1992.
134. Saito Y, Watanabe H. Colony specificity in the compound ascidian Botryllus scalaris. Proc. Japn. Acad. 58B: 105-108, 1982.
135. Saito Y, Watanabe H. Partial biochemical characterization of humoral factors involved in the nonfusion reaction of a botryllid ascidian, Botrylloides simodensis. Zool. Sci. 1: 229-235, 1984.
136. Saito Y, Hirose E, Watanabe H. Allorecognition in compound ascidians. Int. J. Dev. Biol. 38: 237-247, 1994.
137. Scofield VL, Schlumpberger JM, West LA, Weissman IL Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295: 499-502, 1982.
138. Scofield VL, Schlumpberger JM, Nagashima LS. Morphology and genetics of rejection reactions between oozooids from the tunicate Botryllus schlosseri. Biol. Bull. 165: 733-744, 1983.
139. Sekizawa A, Kimura T, Sasaki M, Nakamura S, Kobayashi R, Sato T. Prenatal Diagnosis of Duchenne Muscular Dystrophy using a Single Fetal Nucleated Erythrocyte in Maternal Blood. Neurology 46: 1350-1353, 1996.
140. Socie G, Gluckman E, Carosella E, Brossard Y, Lafon C, Brison O. Search for maternal cells in human umbilical cord blood by polymerase chain reaction amplification of two minisatellite sequences. Blood 83: 340-344, 1994.
141. Stone WH, Cragle RG, Swanson EW, Brown DG. Skin grafts: Delayed rejection between pairs of cattle twins showing erythrocyte chimerism. Science 148: 1335-1336, 1965.
142. Stone WH, Cragle RG, Johnson DF, Bacon JA, Bendel S, Korda N. Long-term observations of skin grafts between chimeric cattle twins. Transplantation 12: 421-428, 1971.
143. Stoner DS, Weissman IL. Somatic and germ cell parasitism in a colonial ascidian: Possible role for a highly polymorphic allorecognition system. Proc. Natl. Acad. Sci. USA 93: 15254-15259, 1996.
144. Stoner DS, Rinkevich B, Weissman IL. Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc. Natl. Acad. Sci. USA 96: 9148-9153, 1999.
145. Tanaka K, Watanabe H. Allogeneic inhibition in a compound ascidian, Botryllus primigenus oka. I. Processes and features of nonfusion reaction. Cell. Immunol. 7: 410-426, 1973.
146. Taneda Y. Simultaneous occurrence of fusion and nonfusion reaction in two colonies in contact of the compound ascidian Botryllus priminegus. Dev. Comp. Immunol. 9: 371-375, 1985.
147. Tippett P. Blood group chimeras. A review. Vox Sang. 44: 333-359, 1983.
148. van den Boogaardt DEM, van Rood JJ, Roelen DL, Claas FH. The influence of inherited and noninherited parental antigens on outcome after transplantation. Transpl. Int. 19: 360-371, 2006.
149. van Dijk BA, Boomsma DI, de Man AJ. Blood group chimerism in human multiple births is not rare. Am. J. Med. Genet. 61: 264-268, 1996.
150. von Eggeling F, Michel S, Gunther M, Schimmel B, Claussen U. Determination of the origin of single nucleated cells in maternal circulation by means of random PCR and a set of length polymorphisms. Hum. Genet. 99: 266-270, 1997.
151. Voskoboynik A, Weissman IL, Rinkevich B. Stem cells, chimerism, and tolerance: Lessons from mammals and ascidians. In: Rinkevich B, Matranga V (eds), Stem cells in marine organisms, Springer-Verlag [in press].
152. Voskoboynik A, Soen Y, Rinkevich Y, Ueno H, Rosner A, Reshef R, et al. Identification of the endostyle as a stem cell niche in a colonial chordate. Cell Stem Cell 3: 456-464, 2008.
153. Wachtel SS, Sammons D, Twitty G, Utermohlen J, Tolley E, Phillips O, et al. Charge Flow Separation: Quantification of Nucleated Red Blood Cells in Maternal Blood during Pregnancy. Prenat. Diagn. 18: 455-463, 1998.
154. Weissman IL, Saito Y, Rinkevich B. Allorecognition histocompatibility in a protochordate species: Is the relationship to MHC somatic or structural?. Immunol. Rev. 113: 227-241, 1990.
155. Zhao Y, Ohdan H, Manilay JO, Sykes M. NK cell tolerance in mixed allogeneic chimeras. J. Immunol. 170: 5398-5405, 2003.