A novel perivascular cell population in the zebrafish brain

eLife

Volumn 6, Issue , 2017, Pages

  Galanternik, Marina Venero ^a   Castranova, Daniel ^a   Gore, Aniket V ^a   Blewett, Nathan H ^a   Jung, Hyun Min ^a   Stratman, Amber N ^a   Kirby, Martha R ^b   Iben, James ^a   Miller, Mayumi F ^a   Kawakami, Koichi ^c,d   Maraia, Richard J ^a   Weinstein, Brant M ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF GENETICS   (Japan)

^d GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; EPIDERMAL GROWTH FACTOR; FLUORESCENT DYE; INDIAN INK; MANNOSE RECEPTOR; MANNOSE RECEPTOR C1 LIKE PROTEIN; MORPHOLINO OLIGONUCLEOTIDE; NEUTRAL RED; SCAVENGER; TRANSCRIPTION FACTOR RUNX; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ADULT; ANGIOGRAPHY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL POPULATION; CHOROID PLEXUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; FLUORESCENT GRANULAR PERITHELIAL CELL; IMMUNOHISTOCHEMISTRY; INTRACRANIAL DRUG ADMINISTRATION; LYMPH VESSEL ENDOTHELIUM; LYMPHOANGIOGRAPHY; MACROPHAGE; MICROANGIOGRAPHY; NONHUMAN; PERIVASCULAR EPITHELIOID CELL TUMOR; PERIVASCULAR MACROPHAGE; PHOTO CONVERSION; PROTEIN EXPRESSION; RNA ISOLATION; RNA SEQUENCE; VASCULAR ENDOTHELIUM; ZEBRA FISH; ANIMAL; BLOOD VESSEL; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; ENDOTHELIUM CELL;

ANIMALS; BLOOD VESSELS; BLOOD-BRAIN BARRIER; BRAIN; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; ZEBRAFISH;

EID: 85019721514     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.24369     Document Type: Article

References (98)

1. Abtin A, Jain R, Mitchell AJ, Roediger B, Brzoska AJ, Tikoo S, Cheng Q, Ng LG, Cavanagh LL, von Andrian UH, Hickey MJ, Firth N, Weninger W. 2014. Perivascular macrophages mediate neutrophil recruitment during bacterial skin infection. Nature Immunology 15:45–53. doi: 10.1038/ni.2769, PMID: 24270515
2. Alders M, Hogan BM, Gjini E, Salehi F, Al-Gazali L, Hennekam EA, Holmberg EE, Mannens MM, Mulder MF, Offerhaus GJ, Prescott TE, Schroor EJ, Verheij JB, Witte M, Zwijnenburg PJ, Vikkula M, Schulte-Merker S, Hennekam RC. 2009. Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nature Genetics 41:1272–1274. doi: 10.1038/ng.484, PMID: 19935664
3. Aoki Y, Saint-Germain N, Gyda M, Magner-Fink E, Lee YH, Credidio C, Saint-Jeannet JP. 2003. Sox10 regulates the development of neural crest-derived melanocytes in xenopus. Developmental Biology 259:19–33. doi: 10.1016/S0012-1606(03)00161-1, PMID: 12812785
4. Apostolopoulos V, McKenzie IF. 2001. Role of the mannose receptor in the immune response. Current Molecular Medicine 1:469–474. doi: 10.2174/1566524013363645, PMID: 11899091
5. Armer JM, Stewart BR. 2005. A comparison of four diagnostic criteria for lymphedema in a post-breast Cancer population. Lymphatic Research and Biology 3:208–217. doi: 10.1089/lrb.2005.3.208, PMID: 16379589
6. Astin JW, Haggerty MJ, Okuda KS, Le Guen L, Misa JP, Tromp A, Hogan BM, Crosier KE, Crosier PS. 2014. Vegfd can compensate for loss of Vegfc in zebrafish facial lymphatic sprouting. Development 141:2680–2690. doi: 10.1242/dev.106591, PMID: 24903752
7. Audoy-Rémus J, Richard JF, Soulet D, Zhou H, Kubes P, Vallières L. 2008. Rod-Shaped monocytes patrol the brain vasculature and give rise to perivascular macrophages under the influence of proinflammatory cytokines and angiopoietin-2. Journal of Neuroscience 28:10187–10199. doi: 10.1523/JNEUROSCI.3510-08.2008, PMID: 18842879
8. Ballabh P, Braun A, Nedergaard M. 2004. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiology of Disease 16:1–13. doi: 10.1016/j.nbd.2003.12.016, PMID: 15207256
9. Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM. 2007. Functionally specialized junctions between endothelial cells of lymphatic vessels. The Journal of Experimental Medicine 204:2349–2362. doi: 10.1084/jem.20062596, PMID: 17846148
10. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. 2010. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464:108–111. doi: 10.1038/nature08738, PMID: 20154733
11. Bhatt S, Diaz R, Trainor PA. 2013. Signals and switches in mammalian neural crest cell differentiation. Cold Spring Harbor Perspectives in Biology 5:a008326. doi: 10.1101/cshperspect.a008326, PMID: 23378583
12. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C. 2010. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464:116–120. doi: 10.1038/nature08764, PMID: 20154729
13. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi: 10.1093/bioinformatics/btu170, PMID: 24695404
14. Bresciani E, Carrington B, Wincovitch S, Jones M, Gore AV, Weinstein BM, Sood R, Liu PP. 2014. Cbfb and RUNX1 are required at 2 different steps during the development of hematopoietic stem cells in zebrafish. Blood 124:70–78. doi: 10.1182/blood-2013-10-531988, PMID: 24850758
15. Bronner ME, LeDouarin NM. 2012. Development and evolution of the neural crest: an overview. Developmental Biology 366:2–9. doi: 10.1016/j.ydbio.2011.12.042, PMID: 22230617
16. Bronner ME. 2012. Formation and migration of neural crest cells in the vertebrate embryo. Histochemistry and Cell Biology 138:179–186. doi: 10.1007/s00418-012-0999-z, PMID: 22820859
17. Burke Z, Oliver G. 2002. Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mechanisms of Development 118:147–155. doi: 10.1016/S0925-4773(02)00240-X, PMID: 12351178
18. Carney TJ, Dutton KA, Greenhill E, Delfino-Machín M, Dufourcq P, Blader P, Kelsh RN. 2006. A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133:4619–4630. doi: 10.1242/dev.02668, PMID: 17065232
19. Covassin LD, Siekmann AF, Kacergis MC, Laver E, Moore JC, Villefranc JA, Weinstein BM, Lawson ND. 2009. A genetic screen for vascular mutants in zebrafish reveals dynamic roles for Vegf/Plcg1 signaling during artery development. Developmental Biology 329:212–226. doi: 10.1016/j.ydbio.2009.02.031, PMID: 19269286
20. Covassin LD, Villefranc JA, Kacergis MC, Weinstein BM, Lawson ND. 2006. Distinct genetic interactions between multiple vegf receptors are required for development of different blood vessel types in zebrafish. PNAS 103: 6554–6559. doi: 10.1073/pnas.0506886103, PMID: 16617120
21. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. doi: 10.1093/bioinformatics/bts635, PMID: 23104886
22. Dutton KA, Pauliny A, Lopes SS, Elworthy S, Carney TJ, Rauch J, Geisler R, Haffter P, Kelsh RN. 2001. Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128:4113–4125. PMID: 11684650
23. Dyer MA, Livesey FJ, Cepko CL, Oliver G. 2003. Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nature Genetics 34:53–58. doi: 10.1038/ng1144, PMID: 12692551
24. Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ. 2011. mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117:e49–e56. doi: 10.1182/blood-2010-10-314120, PMID: 21084707
25. Faraco G, Sugiyama Y, Lane D, Garcia-Bonilla L, Chang H, Santisteban MM, Racchumi G, Murphy M, Van Rooijen N, Anrather J, Iadecola C. 2016. Perivascular macrophages mediate the neurovascular and cognitive dysfunction associated with hypertension. Journal of Clinical Investigation 126:4674–4689. doi: 10.1172/JCI86950, PMID: 27841763
26. Gazi U, Martinez-Pomares L. 2009. Influence of the mannose receptor in host immune responses. Immunobiology 214:554–561. doi: 10.1016/j.imbio.2008.11.004, PMID: 19162368
27. Gérard C, Bleyzac N, Girard P, Freyer G, Bertrand Y, Tod M. 2010. Influence of dosing schedule on organ exposure to cyclosporin in pediatric hematopoietic stem cell transplantation: analysis with a PBPK model. Pharmaceutical Research 27:2602–2613. doi: 10.1007/s11095-010-0252-1, PMID: 20811933
28. Gore AV, Athans B, Iben JR, Johnson K, Russanova V, Castranova D, Pham VN, Butler MG, Williams-Simons L, Nichols JT, Bresciani E, Feldman B, Kimmel CB, Liu PP, Weinstein BM. 2016. Epigenetic regulation of hematopoiesis by DNA methylation. eLife 5:e11813. doi: 10.7554/eLife.11813, PMID: 26814702
29. Hall C, Flores MV, Storm T, Crosier K, Crosier P. 2007. The zebrafish lysozyme C promoter drives myeloid-specific expression in transgenic fish. BMC Developmental Biology 7:42. doi: 10.1186/1471-213X-7-42, PMID: 17477879
30. Hatta K, Tsujii H, Omura T. 2006. Cell tracking using a photoconvertible fluorescent protein. Nature Protocols 1: 960–967. doi: 10.1038/nprot.2006.96, PMID: 17406330
31. He H, Mack JJ, Guc E, Warren CM, Squadrito ML, Kilarski WW, Baer C, Freshman RD, McDonald AI, Ziyad S, Swartz MA, De Palma M, Iruela-Arispe ML. 2016. Perivascular macrophages Limit Permeability. Arteriosclerosis, Thrombosis, and Vascular Biology 36:2203–2212. doi: 10.1161/ATVBAHA.116.307592, PMID: 27634833
32. Herbomel P, Thisse B, Thisse C. 2001. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Developmental Biology 238:274–288. doi: 10.1006/dbio.2001.0393, PMID: 11784010
33. Hogan BM, Bos FL, Bussmann J, Witte M, Chi NC, Duckers HJ, Schulte-Merker S. 2009. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nature Genetics 41:396–398. doi: 10.1038/ng.321, PMID: 19287381
34. Hong YK, Detmar M. 2003. Prox1, master regulator of the lymphatic vasculature phenotype. Cell and Tissue Research 314:85–92. doi: 10.1007/s00441-003-0747-8, PMID: 12883994
35. Hong YK, Harvey N, Noh YH, Schacht V, Hirakawa S, Detmar M, Oliver G. 2002. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Developmental Dynamics 225:351–357. doi: 10.1002/dvdy.10163, PMID: 12412020
36. Honore´ SM, Aybar MJ, Mayor R. 2003. Sox10 is required for the early development of the prospective neural crest in xenopus embryos. Developmental Biology 260:79–96. doi: 10.1016/S0012-1606(03)00247-1, PMID: 12885557
37. Isogai S, Horiguchi M, Weinstein BM. 2001. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Developmental Biology 230:278–301. doi: 10.1006/dbio.2000.9995, PMID: 11161578
38. Jais A, Solas M, Backes H, Chaurasia B, Kleinridders A, Theurich S, Mauer J, Steculorum SM, Hampel B, Goldau J, Alber J, Förster CY, Eming SA, Schwaninger M, Ferrara N, Karsenty G, Brüning JC. 2016. Myeloid-Cell-Derived VEGF maintains brain glucose uptake and limits cognitive impairment in obesity. Cell 165:882–895. doi: 10.1016/j.cell.2016.03.033, PMID: 27133169
39. Jing L, Zon LI. 2011. Zebrafish as a model for normal and malignant hematopoiesis. Disease Models & Mechanisms 4:433–438. doi: 10.1242/dmm.006791, PMID: 21708900
40. Johnson NC, Dillard ME, Baluk P, McDonald DM, Harvey NL, Frase SL, Oliver G. 2008. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes & Development 22:3282–3291. doi: 10./gad.1727208, PMID: 19056883
41. Jung HM, Castranova D, Swift MR, Pham VN, Venero Galanternik M, Isogai S, Butler MG, Mulligan TS, Weinstein BM. 2017. Development of the larval lymphatic system in the zebrafish. Development. In press. doi: 10.1242/dev.145755
42. Kawakami K, Abe G, Asada T, Asakawa K, Fukuda R, Ito A, Lal P, Mouri N, Muto A, Suster ML, Takakubo H, Urasaki A, Wada H, Yoshida M. 2010. zTrap: zebrafish gene trap and enhancer trap database. BMC Developmental Biology 10:105. doi: 10.1186/1471-213X-10-105, PMID: 20950494
43. Kikuchi K, Holdway JE, Werdich AA, Anderson RM, Fang Y, Egnaczyk GF, Evans T, Macrae CA, Stainier DY, Poss KD. 2010. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464:601–605. doi: 10.1038/nature08804, PMID: 20336144
44. Kissa K, Herbomel P. 2010. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464:112–115. doi: 10.1038/nature08761, PMID: 20154732
45. Knight RD, Schilling TF. 2006. Cranial neural crest and development of the head skeleton. Advances in Experimental Medicine and Biology 589:120–133. doi: 10.1007/978-0-387-46954-6_7, PMID: 17076278
46. Kopinke D, Sasine J, Swift J, Stephens WZ, Piotrowski T. 2006. Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification. Developmental Dynamics 235:2695–2709. doi: 10.1002/dvdy.20905, PMID: 16871626
47. wan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB. 2007. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Developmental Dynamics 236:3088–3099. doi: 10.1002/dvdy.21343, PMID: 17937395
48. Lam EY, Hall CJ, Crosier PS, Crosier KE, Flores MV. 2010. Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells. Blood 116:909–914. doi: 10.1182/blood-2010-01-264382, PMID: 20453160
49. Le Guyader D, Redd MJ, Colucci-Guyon E, Murayama E, Kissa K, Briolat V, Mordelet E, Zapata A, Shinomiya H, Herbomel P. 2008. Origins and unconventional behavior of neutrophils in developing zebrafish. Blood 111:132–141. doi: 10.1182/blood-2007-06-095398, PMID: 17875807
50. Lee S, Kang J, Yoo J, Ganesan SK, Cook SC, Aguilar B, Ramu S, Lee J, Hong YK. 2009. Prox1 physically and functionally interacts with COUP-TFII to specify lymphatic endothelial cell fate. Blood 113:1856–1859. doi: 10.1182/blood-2008-03-145789, PMID: 18815287
51. Linehan SA, Martinez-Pomares L, Gordon S. 2000. Mannose receptor and scavenger receptor: two macrophage pattern recognition receptors with diverse functions in tissue homeostasis and host defense. Advances in Experimental Medicine and Biology 479:1–14. doi: 10.1007/0-306-46831-X_1, PMID: 10897405
52. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J. 2015. Structural and functional features of central nervous system lymphatic vessels. Nature 523:337–341. doi: 10.1038/nature14432, PMID: 26030524
53. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15:550. doi: 10.1186/s13059-014-0550-8, PMID: 25516281
54. Marquart GD, Tabor KM, Brown M, Strykowski JL, Varshney GK, LaFave MC, Mueller T, Burgess SM, Higashijima S, Burgess HA. 2015. A 3D Searchable Database of Transgenic Zebrafish Gal4 and Cre Lines for Functional Neuroanatomy Studies. Frontiers in Neural Circuits 9:78. doi: 10.3389/fncir.2015.00078, PMID: 26635538
55. Mato M, Aikawa E, Mato TK, Kurihara K. 1986a. Tridimensional observation of fluorescent granular perithelial (FGP) cells in rat cerebral blood vessels. The Anatomical Record 215:413–419. doi: 10.1002/ar.1092150413, PMID: 3740477
56. Mato M, Mato TK. 1983. Distribution and number of fluorescent granular perithelial cells in coronal sections of rats cerebrum. Experientia 39:1374–1376. doi: 10.1007/BF01990111, PMID: 6653725
57. Mato M, Ookawara S, Aikawa E, Kawasaki K. 1981. Studies on fluorescent granular perithelium (F.G.P.) of rat cerebral cortex - especially referring to morphological changes in aging. Anatomischer Anzeiger 149:486–501. PMID: 6974517
58. Mato M, Ookawara S, Mato TK, Namiki T. 1985. An attempt to differentiate further between microglia and fluorescent granular perithelial (FGP) cells by their capacity to incorporate exogenous protein. American Journal of Anatomy 172:125–140. doi: 10.1002/aja.1001720203, PMID: 3976543
59. Mato M, Ookawara S, Saito-Taki T. 1986b. Serological determinants of fluorescent granular perithelial cells along small cerebral blood vessels in rodent. Acta Neuropathologica 72:117–123. doi: 10.1007/BF00685972, PMID: 2435105
60. Mato M, Ookawara S, Sakamoto A, Aikawa E, Ogawa T, Mitsuhashi U, Masuzawa T, Suzuki H, Honda M, Yazaki Y, Watanabe E, Luoma J, Yla-Herttuala S, Fraser I, Gordon S, Kodama T. 1996. Involvement of specific macrophage-lineage cells surrounding arterioles in barrier and scavenger function in brain cortex. PNAS 93: 3269–3274. doi: 10.1073/pnas.93.8.3269, PMID: 8622926
61. Mato M, Ookawara S, Sakamoto A. 1997. Growth retardation of Mato’s fluorescent granular perithelial (FGP) cells in scavenger receptor knockout (SRKO) mice. The Anatomical Record 247:307–316. doi: 10.1002/(SICI)1097-0185(199703)247:3<307::AID-AR2>3.0.CO;2-R, PMID: 9066908
62. Mato M, Ookawara S, Sano M, Fukuda S, Sokabe H. 1983. Behavior of fluorescent granular perithelium (FGP) in cerebral cortex of SHR-SP rats under some conditions. Experimental and Molecular Pathology 39:100–109. doi: 10.1016/0014-4800(83)90044-8, PMID: 6307741
63. Mato M, Ookawara S, Sano M, Fukuda S. 1982a. Uptake of fat by fluorescent granular perithelial cells in cerebral cortex after administration of fat rich chow. Experientia 38:1496–1498. doi: 10.1007/BF01955791, PMID: 7151978
64. Mato M, Ookawara S, Sano M, Kurihara K. 1982b. [Studies on cerebral scavenger cells (fluorescent granular perithelial cells) - especially uptake and digestion of incorporated fat]. No to Shinkei = Brain and Nerve 34:989–997. PMID: 6924858
65. Mato M, Ookawara S, Sugamata M, Aikawa E. 1984. Evidence for the possible function of the fluorescent granular perithelial cells in brain as scavengers of high-molecular-weight waste products. Experientia 40:399–402. doi: 10.1007/BF01952574, PMID: 6325229
66. Mato M, Ookawara S. 1979. A simple method for observation of capillary nets in rat brain cortex. Experientia 35: 501–503. doi: 10.1007/BF01922731, PMID: 437032
67. Mato M, Ookawara S. 1981. Influences of age and vasopressin on the uptake capacity of fluorescent granular perithelial cells (FGP) of small cerebral vessels of the rat. American Journal of Anatomy 162:45–53. doi: 10.1002/aja.1001620105, PMID: 7304474
68. Mato M, Sakamoto A, Ookawara S, Takeuchi K, Suzuki K. 1998. Ultrastructural and immunohistochemical changes of fluorescent granular perithelial cells and the interaction of FGP cells to microglia after lipopolysaccharide administration. The Anatomical Record 251:330–338. doi: 10.1002/(SICI)1097-0185(199807)251:3<330::AID-AR8>3.0.CO;2-Z, PMID: 9669760
69. Mato M, Takeuchi K, Ookawara S, Yamanaka S, Mashiko T, Ogura K. 2002. Inclusions in novel perivascular macrophages (Mato’s fluorescent granular perithelial cells) and neurons in the cerebral cortex of Hex A- and Hex B-deficient mice. Acta Neuropathologica 103:119–130. doi: 10.1007/s004010100441, PMID: 11810177
70. Mendes-Jorge L, Ramos D, Luppo M, Llombart C, Alexandre-Pires G, Nacher V, Melgarejo V, Correia M, Navarro M, Carretero A, Tafuro S, Rodriguez-Baeza A, Esperança-Pina JA, Bosch F, Ruberte J. 2009. Scavenger function of resident autofluorescent perivascular macrophages and their contribution to the maintenance of the blood-retinal barrier. Investigative Opthalmology & Visual Science 50:5997–6005. doi: 10.1167/iovs.09-3515, PMID: 19608545
71. Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, Lin HF, Handin RI, Herbomel P. 2006. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25:963–975. doi: 10.1016/j.immuni.2006.10.015, PMID: 17157041
72. North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR, Lord AM, Weber GJ, Bowman TV, Jang IH, Grosser T, Fitzgerald GA, Daley GQ, Orkin SH, Zon LI. 2007. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447:1007–1011. doi: 10.1038/nature05883, PMID: 17581586
73. Okuda KS, Astin JW, Misa JP, Flores MV, Crosier KE, Crosier PS. 2012. lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development 139:2381–2391. doi: 10.1242/dev.077701, PMID: 22627281
74. Oliver G, Harvey N. 2002. A stepwise model of the development of lymphatic vasculature. Annals of the New York Academy of Sciences 979:159–165. doi: 10.1111/j.1749-6632.2002.tb04876.x, PMID: 12543725
75. Ookawara S, Mitsuhashi U, Suminaga Y, Mato M. 1996. Study on distribution of pericyte and fluorescent granular perithelial (FGP) cell in the transitional region between arteriole and capillary in rat cerebral cortex. The Anatomical Record 244:257–204. doi: 10.1002/(SICI)1097-0185(199602)244:2<257::AID-AR13>3.0.CO;2-O, PMID: 8808400
76. Op den Brouw ML, Binda RS, Geijtenbeek TB, Janssen HL, Woltman AM. 2009. The mannose receptor acts as hepatitis B virus surface antigen receptor mediating interaction with intrahepatic dendritic cells. Virology 393: 84–90. doi: 10.1016/j.virol.2009.07.015, PMID: 19683778
77. Paratore C, Goerich DE, Suter U, Wegner M, Sommer L. 2001. Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling. Development 128:3949–3961. PMID: 11641219
78. Peyrot SM, Martin BL, Harland RM. 2010. Lymph heart musculature is under distinct developmental control from lymphatic endothelium. Developmental Biology 339:429–438. doi: 10.1016/j.ydbio.2010.01.002, PMID: 20067786
79. Poage E, Singer M, Armer J, Poundall M, Shellabarger MJ. 2008. Demystifying lymphedema: development of the lymphedema putting evidence into practice card. Clinical Journal of Oncology Nursing 12:951–964. doi: 10.1188/08.CJON.951-964, PMID: 19064389
80. Renshaw SA, Loynes CA, Trushell DM, Elworthy S, Ingham PW, Whyte MK. 2006. A transgenic zebrafish model of neutrophilic inflammation. Blood 108:3976–3978. doi: 10.1182/blood-2006-05-024075, PMID: 16926288
81. Rhodes J, Hagen A, Hsu K, Deng M, Liu TX, Look AT, Kanki JP. 2005. Interplay of pu.1 and gata1 determines myelo-erythroid progenitor cell fate in zebrafish. Developmental Cell 8:97–108. doi: 10.1016/j.devcel.2004.11.014, PMID: 15621533
82. Risebro CA, Searles RG, Melville AA, Ehler E, Jina N, Shah S, Pallas J, Hubank M, Dillard M, Harvey NL, Schwartz RJ, Chien KR, Oliver G, Riley PR. 2009. Prox1 maintains muscle structure and growth in the developing heart. Development 136:495–505. doi: 10.1242/dev.030007, PMID: 19091769
83. Rodriguez-Niedenführ M, Papoutsi M, Christ B, Nicolaides KH, von Kaisenberg CS, Tomarev SI, Wilting J. 2001. Prox1 is a marker of ectodermal placodes, endodermal compartments, lymphatic endothelium and lymphangioblasts. Anatomy and Embryology 204:399–406. doi: 10.1007/s00429-001-0214-9, PMID: 11789987
84. Sauteur L, Krudewig A, Herwig L, Ehrenfeuchter N, Lenard A, Affolter M, Belting HG. 2014. Cdh5/VE-cadherin promotes endothelial cell interface elongation via cortical actin polymerization during angiogenic sprouting. Cell Reports 9:504–513. doi: 10.1016/j.celrep.2014.09.024, PMID: 25373898
85. Shin JW, Min M, Larrieu-Lahargue F, Canron X, Kunstfeld R, Nguyen L, Henderson JE, Bikfalvi A, Detmar M, Hong YK. 2006. Prox1 promotes lineage-specific expression of fibroblast growth factor (FGF) receptor-3 in lymphatic endothelium: a role for FGF signaling in lymphangiogenesis. Molecular Biology of the Cell 17:576–584. doi: 10.1091/mbc.E05-04-0368, PMID: 16291864
86. Sood R, English MA, Belele CL, Jin H, Bishop K, Haskins R, McKinney MC, Chahal J, Weinstein BM, Wen Z, Liu PP. 2010. Development of multilineage adult hematopoiesis in the zebrafish with a runx1 truncation mutation. Blood 115:2806–2809. doi: 10.1182/blood-2009-08-236729, PMID: 20154212
87. Sosa-Pineda B, Wigle JT, Oliver G. 2000. Hepatocyte migration during liver development requires Prox1. Nature Genetics 25:254–255. doi: 10.1038/76996, PMID: 10888866
88. Sweet L, Singh PP, Azad AK, Rajaram MV, Schlesinger LS, Schorey JS. 2010. Mannose receptor-dependent delay in phagosome maturation by Mycobacterium avium glycopeptidolipids. Infection and Immunity 78:518–526. doi: 10.1128/IAI.00257-09, PMID: 19841083
89. Tamplin OJ, Durand EM, Carr LA, Childs SJ, Hagedorn EJ, Li P, Yzaguirre AD, Speck NA, Zon LI. 2015. Hematopoietic stem cell arrival triggers dynamic remodeling of the perivascular niche. Cell 160:241–252. doi: 10.1016/j.cell.2014.12.032, PMID: 25594182
90. Totong R, Schell T, Lescroart F, Ryckebüsch L, Lin YF, Zygmunt T, Herwig L, Krudewig A, Gershoony D, Belting HG, Affolter M, Torres-Vázquez J, Yelon D. 2011. The novel transmembrane protein Tmem2 is essential for coordination of myocardial and endocardial morphogenesis. Development 138:4199–4205. doi: 10.1242/dev.064261, PMID: 21896630
91. van Impel A, Zhao Z, Hermkens DM, Roukens MG, Fischer JC, Peterson-Maduro J, Duckers H, Ober EA, Ingham PW, Schulte-Merker S. 2014. Divergence of zebrafish and mouse lymphatic cell fate specification pathways. Development 141:1228–1238. doi: 10.1242/dev.105031, PMID: 24523456
92. Vanhollebeke B, Stone OA, Bostaille N, Cho C, Zhou Y, Maquet E, Gauquier A, Cabochette P, Fukuhara S, Mochizuki N, Nathans J, Stainier DYR. 2015. Tip cell-specific requirement for an atypical Gpr124- and Reck-dependent wnt/b-catenin pathway during brain angiogenesis. eLife 4:e06489. doi: 10.7554/eLife.06489, PMID: 26051822
93. Wang Y, Kaiser MS, Larson JD, Nasevicius A, Clark KJ, Wadman SA, Roberg-Perez SE, Ekker SC, Hackett PB, McGrail M, Essner JJ. 2010. Moesin1 and Ve-cadherin are required in endothelial cells during in vivo tubulogenesis. Development 137:3119–3128. doi: 10.1242/dev.048785, PMID: 20736288
94. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G. 2002. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. The EMBO Journal 21:1505–1513. doi: 10.1093/emboj/21.7.1505, PMID: 11927535
95. Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769–778. doi: 10.1016/S0092-8674(00)81511-1, PMID: 10499794
96. Williams K, Alvarez X, Lackner AA. 2001. Central nervous system perivascular cells are immunoregulatory cells that connect the CNS with the peripheral immune system. Glia 36:156–164. doi: 10.1002/glia.1105, PMID: 11596124
97. Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein BM. 2006. Live imaging of lymphatic development in the zebrafish. Nature Medicine 12:711–716. doi: 10.1038/nm1427, PMID: 16732279
98. Yokoo H, Isoda K, Sakura M, Sasaki A, Hirato J, Nakazato Y. 2000. A novel monoclonal antibody that recognizes human perivascular cells of the central nervous system under a specific immune reaction. Neuropathology 20: 216–220. doi: 10.1046/j.1440-1789.2000.00345.x, PMID: 11132938