Hostname: page-component-7479d7b7d-pfhbr Total loading time: 0 Render date: 2024-07-12T02:00:03.213Z Has data issue: false hasContentIssue false
  • English
  • Français

Migratory Activities and Stemness Properties of Rodlet Cells

Part of: Micrographia Collection

Published online by Cambridge University Press:  21 August 2020

Hanan H. Abd-Elhafeez Open the ORCID record for Hanan H. Abd-Elhafeez [Opens in a new window] ,
Alaa S. Abou-Elhamd Open the ORCID record for Alaa S. Abou-Elhamd [Opens in a new window] ,
Walied Abdo Open the ORCID record for Walied Abdo [Opens in a new window]  and
Soha A. Soliman Open the ORCID record for Soha A. Soliman [Opens in a new window]
Hanan H. Abd-Elhafeez*
Affiliation:
Department of Anatomy, Embryology and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut71526, Egypt
Alaa S. Abou-Elhamd
Affiliation:
Department of Anatomy, Embryology and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut71526, Egypt
Walied Abdo
Affiliation:
Department of Pathology, Faculty of Veterinary Medicine, Kafr El Sheikh University, Kafr El Sheikh33516, Egypt
Soha A. Soliman
Affiliation:
Department of Histology, Faculty of Veterinary Medicine, South Valley University, Qena83523, Egypt
*
*Author for correspondence: Hanan H. Abd-Elhafeez, E-mail: hhmmzz91@gmail.com.
Get access

Abstract

The current study aimed to characterize different stages of rodlet cells using light microscopy, immunohistochemistry, and transmission electron microscopy. Granular rodlet cells have a distinct granular cytoplasm. Transitional rodlet cells had distinct capsules, and immature granules. Mature rodlet cells were pear-shaped and had elongated granules. Ruptured rodlet cells had a granular cytoplasm. The affinity of rodlet cells for different histochemical techniques was detected. Immunohistochemical analysis of rodlet cells for stem cell markers such as CD117, CD34, proliferation marker, proliferating cell nuclear antigen (PCNA), endopeptidase activity; matrix metalloproteinase-9 (MPP-9) and the angiogenic factor; vascular endothelial growth factor (VEGF) was investigated. All stages of rodlet cells were expressed CD117. However, the ruptured stage was CD117-negative. The granular, transitional, and mature stages had strong CD34 immunoaffinity, while the ruptured rodlet cells were CD34-negative. The most potent immunoreactivity for PCNA was the granular rodlet cells. The transitional cells exhibited less immunoreactivity, while mature rodlet cells had no immunoaffinity for PCNA. All stages of rodlet cells had high enzyme activity as indicated by Acridine orange and exhibited strong MPP-9 immunoaffinity. VEGF is mostly expressed by granular, transitional, and mature rodlet cells. In conclusion, rodlet cells relatively had stemness properties, endopeptidase activity, express a proliferation marker, and angiogenic factors. We suggest a potential role of rodlet cells in immune defense.

Keywords

CD117 and CD 34MPP-9PCNArodlet cellsVEGF
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 26 , Issue 5 , October 2020 , pp. 1035 - 1052
Check for updates
Copyright
Copyright © Microscopy Society of America 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdelhadi, Z, Naeim, M, El-Wazir, Y, Ibrahim, M & Hosny, S (2015). Histological study on the effect of transplanted human umbilical cord blood CD34+ stem cells on albino rats subjected to myocardial infarction. J Afr Ass Physiol Sci 3(1), 49–57.Google Scholar
Abd-Elhafeez, HH, Abou-Elhamd, AS & Soliman, SA (2020). Morphological and immunohistochemical phenotype of TCs in the intestinal bulb of the Grass carp and their potential role in intestinal immunity. Scientific Reports. doi:10.1038/s41598-020-70032-y.CrossRefGoogle ScholarPubMed
Abd-Elhafeez, HH, Moustafa, MN, Zayed, AE & Sayed, R (2017 a). Morphological and morphometric study of the development of Leydig cell population of donkey (Equus asinus) testis from birth to maturity. Cell Biol 6(1), 2.Google Scholar
Abd-Elhafeez, HH, Moustafa, MN, Zayed, AE & Sayed, R (2017 b). The development of the intratesticular excurrent duct system of donkey (Equus asinus) from birth to maturity. Histol Cytol Embryol 1(2), 6–8. doi:10.15761/HCE.1000108Google Scholar
Abd-Elhafeez, HH & Soliman, SA (2016). Origin of rodlet cells and mapping their distribution in ruby-red-fin shark (rainbow shark) Epalzeorhynchos frenatum (Teleostei: Cyprinidae): Light, immunohistochemistry and ultrastructure study. J Cytol Histol 7, 435.Google Scholar
Abd-Elhafeez, HH & Soliman, SA (2017). New description of telocyte sheaths in the bovine uterine tube: An immunohistochemical and scanning microscopic study. Cells Tissues Organs 203(5), 295–315.CrossRefGoogle ScholarPubMed
Abdel-Hakeem, S, Soliman, SA, Abd-Elhafeez, HH, Abdel-Hafez, E & Zaki, RS (2019 a). Occurrence of metacercarial cyst of Ascocotyle (Ascocotyle sp.) in the gills of ruby-red-fin shark (rainbow shark) Epalzeorhynchos frenatum (Teleostei: Cyprinidae): Light microscopic study. EC Clin Exp Anat 2, 296–304.Google Scholar
Abdel-Hakeem, SS, Mahmoud, GAE & Abdel-Hafeez, HH (2019 b). Evaluation and microanalysis of parasitic and bacterial agents of Egyptian fresh Sushi, Salmo salar. Microsc Microanal 25(6), 1498–1508.CrossRefGoogle ScholarPubMed
Abd-Elkareem, M (2017). Cell-specific immuno-localization of progesterone receptor alpha in the rabbit ovary during pregnancy and after parturition. Anim Reprod Sci 180, 100–120.CrossRefGoogle ScholarPubMed
Abdel-Maksoud, FM, Abd-Elhafeez, HH & Soliman, SA (2019). Morphological changes of telocytes in camel efferent ductules in response to seasonal variations during the reproductive cycle. Sci Rep 9(1), 1–17.CrossRefGoogle ScholarPubMed
Bali, P, Bammidi, S, Banik, A, Nehru, B & Anandn, A (2018). CD34 and CD117 Stemness of lineage-negative cells reverses memory loss induced by amyloid beta in mouse model. Front Behav Neurosci 12(222). https://doi.org/10.3389/fnbeh.CrossRefGoogle ScholarPubMed
Barber, DL, Westermann, JM & Jensen, DN (1979). New observations on the rodlet cell (Rhabdospora thelohani) in the white sucker Catostomus commersoni (Lacépède): LM and EM studies. J Fish Biol 14(3), 277–284.CrossRefGoogle Scholar
Bates, D (2010). Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 87(2), 262–271.CrossRefGoogle ScholarPubMed
Bielek, E (2005). Development of the endoplasmic reticulum in the rodlet cell of two teleost species. Anat Rec A Discov Mol Cell Evol Biol 283(1), 239–249.CrossRefGoogle ScholarPubMed
Bosi, G, DePasquale, JA, Manera, M, Castaldelli, G, Giari, L & Sayyaf Dezfuli, B (2018). Histochemical and immunohistochemical characterization of rodlet cells in the intestine of two teleosts, Anguilla anguilla and Cyprinus carpio. J Fish Dis 41(3), 475–485.CrossRefGoogle ScholarPubMed
Bourne, GH, Danielli, JF & Jeon, KW (1975). International Review of Cytology, vol. 40. Elsevier Science & Technology. New York, San Francisco, London: Academic Press. A Subsidiary of Harcourt Brace]manovich, Publishers.Google Scholar
Bücherl, W, Buckley, EE & Deulofeu, V (Eds.) (2013). Venomous Animals and Their Venoms: Venomous Vertebrates. Elsevier.books.google.com, ISBN:1483263630, 9781483263632.pages 732 .Google Scholar
Clendeninn, NJ & Appelt, K (Eds.) (2000). Matrix Metalloproteinase Inhibitors in Cancer Therapy. New York: Springer Science & Business Media.CrossRefGoogle Scholar
Clerc, S & Barenholz, Y (1998). A quantitative model for using Acridine Orange as a transmembrane pH gradient probe. Anal Biochem 259(1), 104–111.CrossRefGoogle ScholarPubMed
Crossmon, G (1937). A modification of Mallory's connective tissue stain with discussion of the principle involved. Anat Rec 69(1), 33–38.CrossRefGoogle Scholar
Culling, CFA (2013). Handbook of Histopathological and Histochemical Techniques: Including Museum Techniques. London: Burlington Elsevier Science. books.google.com.Google Scholar
Dempsey, EW & Lansing, AI (1954). Elastic tissue. Int Rev Cytol 3, 437–453.CrossRefGoogle Scholar
DePasquale, JA (2020). Tropomyosin and alpha-actinin in teleost rodlet cells. Acta Zool. Accepted article. https://doi.org/10.1111/azo.12344.CrossRefGoogle Scholar
Derler, R, Gesslbauer, B, Weber, C, Strutzmann, E, Miller, I & Kungl, A (2017). Glycosaminoglycan-mediated downstream signaling of CXCL8 binding to endothelial cells. Int J Mol Sci 18(12), 2605.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Capuano, S, Simoni, E, Previati, M & Giari, L (2007). Rodlet cells and the sensory systems in zebrafish (Danio rerio). Ana Rec 290(4), 367–374.CrossRefGoogle Scholar
Dezfuli, BS, Giari, L, Lui, A, Squerzanti, S, Castaldelli, G, Shinn, AP, Manera, M & Lorenzoni, M (2012). Proliferative cell nuclear antigen (PCNA) expression in the intestine of Salmo trutta trutta naturally infected with an acanthocephalan. Parasite Vector 5((1), 198.CrossRefGoogle Scholar
El-Bab, MF, Abdelhafeez, HH, Soliman, SA & Kamal, BM (2019). Identification of tracheal cartilage canals in camel. PSM Vet Res 3, 99–105.Google Scholar
El Dawi, HS, Elgharabawy, GS, El Sharkawy, EE, Moustafa, AE, Amr, IM & Bayomy, OI (2013). Histological studies on skeletal muscles of albino rats under the effect of atorvastatin. Egypt J Hosp Med 53(1), 883–903.CrossRefGoogle Scholar
Fatma El-Zahraa, AM & Abd-Elhafez, EA (2018). A histological, histochemical and ultrastructural characterization of uterine vessels at early stages of pregnancy. J Histol Histopathol Res 2(2), 41–47.Google Scholar
Gartner, LP (2020). Textbook of Histology e-Book, 5th ed. Elsevier Health Sciences, p. 704. ISBN 9780323672726Google Scholar
Gartner, LP & Hiatt, JL (2006). Color Textbook of Histology e-Book. Elsevier. 592 pagesGoogle Scholar
Gates, L, Adler, RR & Elangbam, CS (2016). Osmium tetroxide post-fixation and periodic acid-Schiff dual-staining technique to demonstrate intracellular lipid and glycogen in the mouse liver section – a novel method for co-visualization of intracellular contents in paraffin-embedded tissue. J Histotechnol 39(1), 2–7. doi:10.1080/01478885.2015.1106072.CrossRefGoogle Scholar
Gharravi, AM, et al. (2007). Effects modification of iron hematoxylin on neuron staining. Pak J Biol Sci 10(5), 768–772.CrossRefGoogle ScholarPubMed
Giari, L, Manera, M, Simoni, E & Dezfuli, BS (2006). Changes to chloride and rodlet cells in gills, kidney and intestine of Dicentrarchus labrax (L.) exposed to reduced salinities. J Fish Biol 69(2), 590–600.CrossRefGoogle Scholar
Gross, CA, Reddy, CK & Dazzo, FB (2010). CMEIAS color segmentation: An improved computing technology to process color images for quantitative microbial ecology studies at single-cell resolution. Microb Ecol 59(2), 400–414.CrossRefGoogle ScholarPubMed
Grover, TR, Zenge, JP, Parker, TA & Abman, SH (2002). Vascular endothelial growth factor causes pulmonary vasodilation through activation of the phosphatidylinositol-3-kinase-nitric oxide pathway in the late-gestation ovine fetus. Pediatr Res 52(6), 907–912.CrossRefGoogle ScholarPubMed
Harris, HF (1900). On the rapid conversion of haematoxylin into haematein in staining reactions. J Appl Microsc Lab Methods 3, 777–780.Google Scholar
Hawkins, WE (1984). Ultrastructure of rodlet cells: response to cadmium damage in the kidney of the spot Leiostomus xanthurus Lacépède. Gulf Res Rep 7(4), 365–372.Google Scholar
Heidenhain, N (1896). Once again about the presentation of centralkorper fabren by Eisenhamatoxylin together with some general Bemer depressions over the hematoxylin. Zeitchr wissen Microsc Mukroskopichtechnol 13, 180.Google Scholar
Hoeben, AN, Landuyt, B, Highley, MS, Wildiers, H, Van Oosterom, AT & De Bruijn, EA (2004). Vascular endothelial growth factor and angiogenesis. Pharmacol Rev 56(4), 549–580.CrossRefGoogle ScholarPubMed
Hoff, RG, Newman, DE & Staneck, JL (1985). Bacteriuria screening by use of acridine orange-stained smears. J Clin Microbiol 21(4), 513–516.CrossRefGoogle ScholarPubMed
Hsu, SM, Raine, L & Fanger, HX (1981). Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29(4), 577–580.CrossRefGoogle ScholarPubMed
Iger, Y & Abraham, M (1997). Rodlet cells in the epidermis of fish exposed to stressors. Tissue Cell 29(4), 431–438.CrossRefGoogle ScholarPubMed
Kamal, EHA, Abdelhafeez, HH, Gaber, W & Tamam, E (2019). Identification of rodlet cells in aquatic bird as Egyptian Goose (Alopochen Aegyptiacus): The enteric rodlet cells. Cytol Histol Int J 3(1), 000108.Google Scholar
Kämmerer, U, Kapp, M, Gassel, AM, Richter, T, Tank, C, Dietl, J & Ruck, P (2001). A new rapid immunohistochemical staining technique using the EnVision antibody complex. J Histochem Cytochem 49(5), 623–630.CrossRefGoogle ScholarPubMed
Karnovsky, MJ (1965). A Formaldehyde-glutaraldehyde fixative of high osmolarity for use electron microscopy. Cell Biol 27(137 A).Google Scholar
Kierszenbaum, AL & Tres, L (2015). Histology and Cell Biology: An Introduction to Pathology E-Book, 4th ed. New York: Saunders, Elsevier Health Sciences, p. 752,eBook. ISBN: 9780323313353Google Scholar
Kiriakidis, S, Andreakos, E, Monaco, C, Foxwell, B, Feldmann, M & Paleolog, E (2003). VEGF expression in human macrophages is NF-κB-dependent: Studies using adenoviruses expressing the endogenous NF-κB inhibitor IκBα and a kinase-defective form of the IκB kinase 2. J Cell Sci 116(4), 665–674.CrossRefGoogle Scholar
Leino, R (1982). Rodlet cells in the gill and intestine of Catostomus commersoni and Perca flavescens: A comparison of their light and electron microscopic cytochemistry with that of mucous and granular cells. Canadian J Zool 60(11), 2768–2782.CrossRefGoogle Scholar
Liao, Z, Cao, C, Wang, J, Huxley, VH, Baker, O, Weisman, GA & Erb, L (2014). The P2Y2 receptor interacts with VE-Cadherin and VEGF receptor-2 to regulate Rac1 activity in endothelial cells. J Biomed Sci Eng 7(14), 1105–1121.CrossRefGoogle ScholarPubMed
Lisa, G, Rick, RA & Chandikumar, SE (2016). Osmium tetroxide post-fixation and periodicacid-Schiff dual-staining technique to demonstrate intracellular lipid andglycogen in the mouse liver section - a novel method for co-visualization ofintracellular contents in paraffin-embedded tissue. J Histotechnol 39(1), 2–7.Google Scholar
Lloyd, RV (2001). Morphology Methods: Cell and Molecular Biology Techniques. New York: Humana Press, Springer Science & Business Media.CrossRefGoogle Scholar
Mackie, AR & Losordo, DW (2011). CD34-positive stem cells: in the treatment of heart and vascular disease in human beings. Texas Heart Institute J 38(5), 474–485.Google ScholarPubMed
Mahmoud, MAM, Zaki, RS & Abd-Elhafeez, HH (2020). An epifluorescencebased technique accelerates risk assessment of aggregated bacterial communities in carcass and environment. Environ Pollut 260, 113950.CrossRefGoogle ScholarPubMed
Mallory, FB (1936). A staining method for mucoids and some other substances in tissues. Stain Technol 11, 101.CrossRefGoogle Scholar
Mayberry, LF, Marchiondo, AA, Ubelaker, JE & Kazić, D (1979). Rhabdospora thelohani Laguessé, 1895 (Apicomplexa): New host and geographic records with taxonomic considerations. J Protozool 26(2), 168–178.CrossRefGoogle ScholarPubMed
McManus, JFA (1948). Histological and histochemical uses of periodic acid. Stain Technol 23(3), 99–108.CrossRefGoogle ScholarPubMed
Melton, D (2014). Chapter 2: ‘Stemness’: definitions, criteria, and standards. In Essentials of Stem Cell Biology, 3rd ed. Lanza, R & Atala, A (Eds.), Boston, MA: Academic Press, pp. 7–17.CrossRefGoogle Scholar
Mokhtar, DM & Abd-Elhafeez, HH (2014). Light-and electron-microscopic studies of olfactory organ of Red-tail shark, Epalzeorhynchos bicolor (Teleostei: Cyprinidae). J Microsc Ultrastruct 2(3), 182–195.CrossRefGoogle Scholar
Monsonego-Ornan, E, Kosonovsky, J, Bar, A, Roth, L, Fraggi-Rankis, V, Simsa, S, Kohl, A & Sela-Donenfeld, D (2012). Matrix metalloproteinase 9/gelatinase B is required for neural crest cell migration. Dev Biol 364(2), 162–177.CrossRefGoogle ScholarPubMed
Moustafa, MNK, Sayed, R, Zayed, AE & AbdEl-Hafeez, HH (2015). Morphological and morphometric study of the development of seminiferous epithelium of donkey (Equus asinus) from birth to maturity. J Cytol Histol 6(6), 1.Google Scholar
Mowry, RW (1963). The special value of methods that color both acidic and vicinal hydroxyl groups in the histochemical study of mucins, with revised directions for the colloidal iron stain, and the use of Alcian blue 8GX and their combinations with the periodic acid-Schiff reaction. 3. Ann New York Acad Sci 106(2), 402–442.CrossRefGoogle Scholar
Murakami, M & Simons, M (2009). Regulation of vascular integrity. J Molecul Med 87(6), 571–582.CrossRefGoogle ScholarPubMed
Mustafa, F & El-Desoky, S (2020). Architecture and cellular composition of the spleen in the Japanese Quail (Coturnix japonica). Microsco Microanal 1–10. doi:10.1017/S143192762000152X.Google Scholar
Mustafa, FE (2019). Putative primo-vascular system in rabbit placenta. J Acupunct Meridian Stud 12(1), 20–24.CrossRefGoogle ScholarPubMed
Nadrigny, F, Li, D, Kemnitz, K, Ropert, N, Koulakoff, A, Rudolph, S, Vitali, M, Giaume, C, Kirchhoff, F & Oheim, M (2007). Systematic colocalization errors between acridine orange and EGFP in astrocyte vesicular organelles. Biophys J 93(3), 969–980.CrossRefGoogle ScholarPubMed
Narzhny, SN (2008). Proliferating cell nuclear antigen: A proteomics view. Cell Mol Life Sci 65(23), 3789–3808.CrossRefGoogle Scholar
Ostrander, GK (2000). “ The Laboratory Fish.” Handbook of Experimental Animals. Washington, USA: Academic press, p. 288.Google Scholar
Reite, OB & Evensen, O (2006). Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunol 20(2), 192–208.CrossRefGoogle ScholarPubMed
Reynolds, EG (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17, 208–212.CrossRefGoogle ScholarPubMed
Shaik-Dasthagirisaheb, YB, Varvara, G, Murmura, G, Saggini, A, Potalivo, G, Caraffa, A, Antinolfi, P, Tete, S, Tripodi, D, Conti, F & Cianchetti, E (2013). Vascular endothelial growth factor (VEGF), mast cells and inflammation. Int J Immunopathol Pharmacol 26(2), 327–335.CrossRefGoogle Scholar
Sidney, LE, Branch, MJ, Dunphy, SE, Dua, HS & Hopkinson, A (2014). Concise review: Evidence for CD34 as a common marker for diverse progenitors. Stem Cells 32(6), 1380–1389.CrossRefGoogle ScholarPubMed
Smith, SA, Caceci, T, Marei, HE & El-Habback, HA (2006). Observations on rodlet cells found in the vascular system and extravascular space of angelfish (Pterophyllum scalare). J Fish Biol 46(2), 241–254.CrossRefGoogle Scholar
Smock, RG & Meijers, R (2018). Roles of glycosaminoglycans as regulators of ligand/receptor complexes. Open Biol 8(10), 180026.CrossRefGoogle ScholarPubMed
Sobhy, W, Ghattas, S, et al. (2014). Assessment of proliferative activity by proliferative cell nuclear antigen (PCNA) and anti-Bromodeoxyuridine (BrdU) immunolabeling in the tissues of Japanese Eels (Anguilla japonica). Turk J Fish Aquat Sci 14, 413–419.Google Scholar
Soliman, AS (2018). The growth cartilage and beyond: Absence of medullary bone in silver carp ribs. Mathew J Cytol Histol 2(1), 008.Google Scholar
Soliman, AS & Abd-Elhafeez, HH (2018). Mesenchymal cells. In Cartilage Growth II, 2nd ed. Germany: Scholars’ Press.Google Scholar
Soliman, S (2017 a). Potential role of telocytes in differentiation of embryonic skeletal progenitor cells. SF J Stem Cell 1(1).Google Scholar
Soliman, S (2017 b). Potential role of telocytes in development of embryonic Ganglia. SF J Stem Cell 1(1).Google Scholar
Soliman, SA (2017 c). Telocytes during organogenesis: Relations to nephrogenic cords in mesonephros of quail embryos. Histol Cytol Embryol 1(4), 1–6.Google Scholar
Soliman, SA (2019). Morphological and histochemical description of quail feather development. Anat Rec. doi.org/10,1002/ar.24276Google ScholarPubMed
Soliman, SA & Abd-Elhafeez, HH (2014). Mesenchymal Cells in Cartilage Growth, 1st Ed. LAP LAMBERT Academic Publishing, pp. 1–49. ISBN: 978-3-65964843-4.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2016 a). Are C-KIT, MMP-9 and type II collagen positive undifferentiated cells involved in cartilage growth? A description of unusual interstitial type of cartilage growth. J Cytol Histol 7, 440.CrossRefGoogle Scholar
Soliman, SA & Abd-Elhafeez, HH (2016 b). Mesenchymal cells in cartilage growth and regeneration: An immunohistochemical and electron microscopic study. J Cytol Histol 7, 437.Google Scholar
Soliman, SA, Ahmed, YA & Abdelsabour-Khalaf, M (2016). Histogenesis of the stomach of the pre-hatching quail: A light microscopic study. Anat Sci Int 91(4), 407–418.CrossRefGoogle ScholarPubMed
Soliman, S & Emeish, W (2017). Morphological alternations of intraepithelial and stromal telocytes in response to salinity challenges. bioRxiv. 115881. doi: https://doi.org/10.1101/115881.Google Scholar
Soliman, SA, Hanan Hassan, A & Enas, A (2017). A new mechanism of cartilage growth in mammals “involvement of CD117 positive undifferentiated cells in interstitial growth”. Mathew J Cytol and Histol 1(1), 001.Google Scholar
Soliman, SA, Kamal, BM & Abd-Elhafeez, HH (2019). Cellular invasion and matrix degradation, a different type of matrix-degrading cells in the cartilage of catfish (Clarias gariepinus) and Japanese quail embryos (Coturnix coturnix japonica). Microsc Microanal 25(5), 1283–1292.CrossRefGoogle Scholar
Soliman, SA, Kamal, BM, Abuo-Elhmad, AS & Abd-Elhafeez, HH (2020). Morphological and histochemical characterization of the dermal plates of pleco (Hypostomus plecostomus). Microsc Microanal 1–6. doi:10.1017/S1431927620001476Google Scholar
Suvarna, KS, Layton, C & Bancroft, JD (2013). Bancroft's Theory and Practice of Histological Techniques. Edinburg, London, Melbourne: Churchill Living Stone.Google Scholar
Tachibana, K, Shibata, M, Gonda, K, Matsumoto, Y, Nakajima, T, Abe, N, Ohtake, T, Ohto, H, Kono, K & Takenoshita, S (2017). IL-17 and VEGF are increased and correlated to systemic inflammation, immune suppression, and malnutrition in patients with breast cancer. Eur J Inflamm 15(3), 219–228.CrossRefGoogle Scholar
Tubbs, RS, Rizk, E, Shoja, MM, Loukas, M, Barbaro, N & Spinner, RJ (Eds.) (2015) Nerves and Nerve Injuries Vol 1: History, Embryology, Anatomy, Imaging, and Diagnostics. (Vol. 1, pp. 1–673). Elsevier Ltd. https://doi.org/10.1016/C2012-0-06700-2.Google Scholar
Van Gieson, J (1889). Laboratory notes of technical methods for the nervous system. NY Med J 50, 57–60.Google Scholar
Weigert, C (1898). Uber eine methode zur farbung elastischer fasern. Zentralbl Allg Pathol Anat 9, 289–292.Google Scholar
Wrobel, KH & Moustafa, MN (2000). On the innervation of the donkey testis. Ann Anat 182(1), 13–22.CrossRefGoogle ScholarPubMed
Yamashiro, K, Ishida, S, Usui, T, Kaji, Y, Ogura, Y & Adamis, AP (2003). VEGF dependent leukocyte infiltration and blood-retinal barrier breakdown in endotoxin-induced uveitis. Investig Ophthalmol Vis Sci 44(13), 719–719.Google Scholar
Yang, J, Yan, J & Liu, B (2018). Targeting VEGF/VEGFR to modulate antitumor immunity. Front Immunol 9(3), 978–978.CrossRefGoogle ScholarPubMed
Yashpal, M & Mittal, AK (2014). Serous goblet cells: The protein secreting cells in the oral cavity of a catfish, Rita rita (Hamilton, 1822) (Bagridae, Siluriformes). Tissue Cell 46(1), 9–14.CrossRefGoogle Scholar
Yen, JH, Khayrullina, T & Ganea, D (2008). PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood 111(1), 260–270.CrossRefGoogle ScholarPubMed
Yousef, MS, Abd-Elhafeez, HH, Talukder, AK & Miyamoto, A (2019). Ovulatory follicular fluid induces sperm phagocytosis by neutrophils, but oviductal fluid around oestrus suppresses its inflammatory effect in the buffalo oviduct in vitro. Mol Reprod Dev 86(7), 835–846.CrossRefGoogle ScholarPubMed
Supplementary material: File

Abd-Elhafeez et al. supplementary material

Tables S1-S10

Download Abd-Elhafeez et al. supplementary material(File)
File 25.6 MB