Intussusceptive Lymphangiogenesis in Lymphatic Malformations/Lymphangiomas.
intussusceptive lymphangiogenesis
lymphangiomas
lymphatic malformations
lymphatic vessels
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
11 2019
11 2019
Historique:
received:
29
05
2018
revised:
10
01
2019
accepted:
09
03
2019
pubmed:
23
6
2019
medline:
9
9
2020
entrez:
23
6
2019
Statut:
ppublish
Résumé
Intussusception in lymphatic vessels has received less attention than in blood vessels. In tumors and pseudotumors of blood vessels with intravascular papillary structures, including sinusoidal hemangioma and intravascular papillary endothelial hyperplasia, we observed exuberant intussusceptive angiogenesis, as well as the similarity between papillae (term used by pathologists) and pillars/folds (hallmarks of intussusceptive angiogenesis). A similar response could be expected in lymphangiomas (lymphatic malformations and reactive processes rather than tumors) with papillae. The aim of this work is to assess whether papillae/pillars/folds and associated structures (vessel loops and septa) are present in lymphangiomas, and to establish the characteristics and formation of these structures. For this purpose, we selected lymphangiomas with intraluminal papillae (n = 18), including cystic, cavernous, circumscriptum, and progressive types, of which two cases of each type with a greater number of papillae were used for serial histologic sections and immunohistochemistry. The studies showed a) dilated lymphatic spaces giving rise to lymphatic-lymphatic vascular loops, which dissected and encircled perilymphatic structures (interstitial tissue structures/ITSs and pillars/posts), b) ITSs and pillars, surrounded by anti-podoplanin-positive endothelial cells, protruding into the lymphatic spaces (papillary aspect), and c) splitting, remodeling, linear arrangement, and fusion of papillae/pillars/folds, forming papillary networks and septa. In conclusion, as occurs in blood vessel diseases, the development of lymphatic vessel loops, papillae/pillars/folds, and septa (segmentation) supports intussusceptive lymphangiogenesis and suggests a piecemeal form of intussusception. This intussusceptive lymphangiogenesis in lymphatic diseases can provide a basis for further studies of lymphatic intussusception in other conditions, with clinical and therapeutic implications. Anat Rec, 302:2003-2013, 2019. © 2019 American Association for Anatomy.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2003-2013Subventions
Organisme : Spanish Ministry of Science, Innovation and Universities
ID : SAF2017-84454-R
Pays : International
Informations de copyright
© 2019 American Association for Anatomy.
Références
Ackermann M, Tsuda A, Secomb TW, Mentzer SJ, Konerding MA. 2013. Intussusceptive remodeling of vascular branch angles in chemically-induced murine colitis. Microvasc Res 87:75-82.
Ackermann M, Houdek JP, Gibney BC, Ysasi A, Wagner W, Belle J, Schittny JC, Enzmann F, Tsuda A, Mentzer SJ, et al. 2014. Sprouting and intussusceptive angiogenesis in postpneumonectomy lung growth: mechanisms of alveolar neovascularization. Angiogenesis 17:541-551.
Ackermann M, Kim YO, Wagner WL, Schuppan D, Valenzuela CD, Mentzer SJ, Kreuz S, Stiller D, Wollin L, Konerding MA. 2017. Effects of nintedanib on the microvascular architecture in a lung fibrosis model. Angiogenesis 20:359-372.
Burri PH. 1992. Intussusceptive microvascular growth, a new mechanism of capillary network formation. EXS 61:32-39.
Burri PH, Djonov V. 2002. Intussusceptive angiogenesis--the alternative to capillary sprouting. Mol Aspects Med 23(6S):S1-S27.
Burri PH, Tarek MR. 1990. A novel mechanism of capillary growth in the rat pulmonary microcirculation. Anat Rec 228:35-45.
Burri PH, Hlushchuk R, Djonov V. 2004. Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn 231:474-488.
Caduff JH, Fischer LC, Burri PH. 1986. Scanning electron microscope study of the developing microvasculature in the postnatal rat lung. Anat Rec 216:154-164.
De Spiegelaere W, Casteleyn C, Van den Broeck W, Plendl J, Bahramsoltani M, Simoens P, Djonov V, Cornillie P. 2012. Intussusceptive angiogenesis: a biologically relevant form of angiogenesis. J Vasc Res 49:390-404.
Diaz-Flores L, Gutierrez R, Valladares F, Varela H, Perez M. 1994. Intense vascular sprouting from rat femoral vein induced by prostaglandins E1 and E2. Anat Rec 238:68-76.
Díaz-Flores L, Gutiérrez R, Madrid JF, García-Suárez MP, González-Álvarez MP, Díaz-Flores L Jr, Sáez FJ. 2016. Intravascular papillary endothelial hyperplasia (IPEH). Evidence supporting a piecemeal mode of angiogenesis from vein endothelium, with vein wall neovascularization and papillary formation. Histol Histopathol 31:1271-1279.
Díaz-Flores L, Gutiérrez R, García MDP, Sáez FJ, Díaz-Flores L Jr, Madrid JF. 2017a. Piecemeal mechanism combining sprouting and intussusceptive angiogenesis in intravenous papillary formation induced by PGE2 and Glycerol. Anat Rec (Hoboken). 300:1781-1792.
Díaz-Flores L, Gutiérrez R, García-Suárez MP, Sáez FJ, Gutiérrez E, Valladares F, Carrasco JL, Díaz-Flores L Jr, Madrid JF. 2017b. Morphofunctional basis of the different types of angiogenesis and formation of postnatal angiogenesis-related secondary structures. Histol Histopathol 32:1239-1279.
Díaz-Flores L, Gutiérrez R, García MP, González-Gómez M, Sáez FJ, Díaz-Flores L Jr, Carrasco JL, Madrid JF. 2018a. Sinusoidal hemangioma and intravascular papillary endothelial hyperplasia: Interrelated processes that share a histogenetic piecemeal angiogenic mechanism. Acta Histochem 120:255-262.
Díaz-Flores L, Gutiérrez R, González-Gómez M, García P, Sáez FJ, Díaz-Flores L Jr, Carrasco JL, Madrid JF. 2018b. Segmentation of dilated hemorrhoidal veins in hemorrhoidal disease. Cells Tissues Organs (in press 205:120-128. https://doi.org/10.1159/000489250.
Dill MT, Rothweiler S, Djonov V, Hlushchuk R, Tornillo L, Terracciano L, Meili-Butz S, Radtke F, Heim MH, Semela D. 2012. Disruption of Notch1 induces vascular remodeling, intussusceptive angiogenesis, and angiosarcomas in livers of mice. Gastroenterology 142:967-977.e2.
Dimova I, Hlushchuk R, Makanya A, Styp-Rekowska B, Ceausu A, Flueckiger S, Lang S, Semela D, Le Noble F, Chatterjee S, et al. 2013. Inhibition of Notch signaling induces extensive intussusceptive neo-angiogenesis by recruitment of mononuclear cells. Angiogenesis 16:921-937.
Djonov V, Schmid M, Tschanz SA, Burri PH. 2000. Intussusceptive angiogenesis: its role in embryonic vascular network formation. Circ Res 86:286-292.
Djonov VG, Kurz H, Burri PH. 2002. Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism. Dev Dyn 224:391-402.
Djonov V, Baum O, Burri PH. 2003. Vascular remodeling by intussusceptive angiogenesis. Cell Tissue Res 314:107-117.
Filipovic N, Tsuda A, Lee GS, Miele LF, Lin M, Konerding MA, Mentzer SJ. 2009. Computational flow dynamics in a geometric model of intussusceptive angiogenesis. Microvasc Res 78:286-293.
Föhst S, Wagner W, Ackermann M, Redenbach C, Schladitz K, Wirjadi O, Ysasi AB, Mentzer SJ, Konerding MA. 2015. Three-dimensional image analytical detection of intussusceptive pillars in murine lung. J Microsc 260:326-337.
Gianni-Barrera R, Trani M, Fontanellaz C, Heberer M, Djonov V, Hlushchuk R, Banfi A. 2013. VEGF over-expression in skeletal muscle induces angiogenesis by intussusception rather than sprouting. Angiogenesis 16:123-136.
Gianni-Barrera R, Bartolomeo M, Vollmar B, Djonov V, Banfi A. 2014. Split for the cure: VEGF, PDGF-BB and intussusception in therapeutic angiogenesis. Biochem Soc Trans 42:1637-1642.
Groppa E, Brkic S, Uccelli A, Wirth G, Korpisalo-Pirinen P, Filippova M, Dasen B, Sacchi V, Muraro MG, Trani M, et al. 2018. EphrinB2/EphB4 signaling regulates non-sprouting angiogenesis by VEGF. EMBO Rep. 19:e45054.
Guillou L, Fletcher CD. 2000. Benign lymphangioendothelioma (acquired progressive lymphangioma): a lesion not to be confused with well-differentiated angiosarcoma and patch stage Kaposi's sarcoma: clinicopathologic analysis of a series. Am J Surg Pathol 24:1047-1057.
Hlushchuk R, Styp-Rekowska B, Dzambazi J, Wnuk M, Huynh-Do U, Makanya A, Djonov V. 2017. Endoglin inhibition leads to intussusceptive angiogenesis via activation of factors related to COUP-TFII signaling pathway. PLoS One 12:e0182813.
Konerding MA, Turhan A, Ravnic DJ, Lin M, Fuchs C, Secomb TW, Tsuda A, Mentzer SJ. 2010. Inflammation-induced intussusceptive angiogenesis in murine colitis. Anat Rec (Hoboken). 293:849-857.
Konerding MA, Gibney BC, Houdek JP, Chamoto K, Ackermann M, Lee GS, Lin M, Tsuda A, Mentzer SJ. 2012. Spatial dependence of alveolar angiogenesis in post-pneumonectomy lung growth. Angiogenesis 15:23-32.
Kuo T, Gomez LG. 1979. Papillary endothelial proliferation in cystic lymphangiomas. A lymphatic vessel counterpart of Masson's vegetant intravascular hemangioendothelioma. Arch Pathol Lab Med 103:306-308.
Kuo T, Sayers CP, Rosai J. 1976. Masson's "vegetant intravascular hemangioendothelioma:" a lesion often mistaken for angiosarcoma: study of seventeen cases located in the skin and soft tissues. Cancer 38:1227-1236.
Kurz H, Burri PH, Djonov VG. 2003. Angiogenesis and vascular remodeling by intussusception: from form to function. News Physiol Sci 18:65-70.
Lee GS, Filipovic N, Lin M, Gibney BC, Simpson DC, Konerding MA, Tsuda A, Mentzer SJ. 2011. Intravascular pillars and pruning in the extraembryonic vessels of chick embryos. Dev Dyn 240:1335-1343.
Makanya AN, Hlushchuk R, Djonov VG. 2009. Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling. Angiogenesis 12:113-123.
Mentzer SJ, Konerding MA. 2014. Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 17:499-509.
Miele LF, Turhan A, Lee GS, Lin M, Ravnic D, Tsuda A, Konerding MA, Mentzer SJ. 2009. Blood flow patterns spatially associated with platelet aggregates in murine colitis. Anat Rec (Hoboken). 292:1143-1153.
Paku S, Kopper L, Nagy P. 2005. Development of the vasculature in "pushing-type" liver metastases of an experimental colorectal cancer. Int J Cancer 115:893-902.
Paku S, Dezso K, Bugyik E, Tóvári J, Tímár J, Nagy P, Laszlo V, Klepetko W, Döme B. 2011. A new mechanism for pillar formation during tumor-induced intussusceptive angiogenesis: inverse sprouting. Am J Pathol 179:1573-1585.
Patan S. 2008. Lycat and cloche at the switch between blood vessel growth and differentiation? Circ Res 102:1005-1007.
Patan S, Alvarez MJ, Schittny JC, Burri PH. 1992. Intussusceptive microvascular growth: a common alternative to capillary sprouting. Arch Histol Cytol 55(Suppl):65-75.
Patan S, Haenni B, Burri PH. 1993. Evidence for intussusceptive capillary growth in the chicken chorio-allantoic membrane (CAM). Anat Embryol (Berl) 187:121-130.
Patan S, Munn LL, Jain RK. 1996. Intussusceptive microvascular growth in a human colon adenocarcinoma xenograft: a novel mechanism of tumor angiogenesis. Microvasc Res 51:260-272.
Patan S, Haenni B, Burri PH. 1997. Implementation of intussusceptive microvascular growth in the chicken chorioallantoic membrane (CAM). Microvasc Res 53:33-52.
Patan S, Munn LL, Tanda S, Roberge S, Jain RK, Jones RC. 2001a. Vascular morphogenesis and remodeling in a model of tissue repair: blood vessel formation and growth in the ovarian pedicle after ovariectomy. Circ Res 89:723-731.
Patan S, Tanda S, Roberge S, Jones RC, Jain RK, Munn LL. 2001b. Vascular morphogenesis and remodeling in a human tumor xenograft: blood vessel formation and growth after ovariectomy and tumor implantation. Circ Res 89:732-739.
Ribatti D, Djonov V. 2012. Intussusceptive microvascular growth in tumors. Cancer Lett 316:126-131.
Tsuda A, Turhan A, Konerding M, Ravnic D, Hanidziar D, Lin M, Mentzer SJ. 2009. Bimodal oscillation frequencies of blood flow in the inflammatory colon microcirculation. Anat Rec (Hoboken) 292:65-72.
Turhan A, Tsuda A, Konerding MA, Lin M, Miele L, Lee G, Mentzer SJ. 2008. Effect of intraluminal pillars on particle motion in bifurcated microchannels. In Vitro Cell Dev Biol Anim 44:426-433.
Vimalraj S, Bhuvaneswari S, Lakshmikirupa S, Jyothsna G, Chatterjee S. 2018. Nitric oxide signaling regulates tumor-induced intussusceptive-like angiogenesis. Microvasc Res 119:47-59.