Skip to main content
SpringerLink
Log in

Comparative Characterization of Capsule Mechanical Properties in Mesenteric Lymph Nodes of Young and Aging Bulls

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

The efficiency of the lymph transport system affects not only the balance of the interstitial fluid, but also other aspects of homeostasis. Lymph transport from the interstitial space to the main veins is mainly provided by rhythmic contractions of the lymphatic vascular segments, lymphangions. Meanwhile, the lymphatic vascular network sequentially incorporates the lymph nodes whose role in lymph transport is poorly understood. The aims of this work were to study the length–tension ratio in the bull mesenteric lymph node capsule and to calculate the pressure the lymph nodes are able to generate, as well as to compare the active and passive mechanical characteristics of the lymph node capsule in young and aging bulls. Experiments on isolated lymph node capsules have shown that lymph nodes are highly extensible structures, which allows them to fill readily with lymph even at the peak of lymph formation. Our data show that the bull mesenteric lymph nodes share the ability to regulate lymph flow along them via the intrinsic mechanisms. Smooth muscle cells in the lymph node capsule are sensitive to stretching, as manifested in an increase in the strength of contractions with an increase in capsule stretching. Lymph nodes are able to generate high active pressure with a significant increase in volume and passive pressure. The extensibility of the lymph node capsule and the active pressure developed by the nodes during spontaneous contractions decline in aging vs. young bulls. Thus, we provide here the first measurements and analysis of the capsular length–tension and nodular diameter–pressure ratios in the mesenteric lymph nodes of young and aging bulls.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.

Similar content being viewed by others

REFERENCES

  1. Lobov GI (2022) The lymphatic system in normal and pathological conditions. Progress Physiol Sci 53: 15–38. https://doi.org/10.31857/S0301179822020060

    Article  Google Scholar 

  2. Liao S, von der Weid PY (2015) Lymphatic system: an active pathway for immune protection. Semin Cell Dev Biol 38: 83–89. https://doi.org/10.1016/j.semcdb.2014.11.012

    Article  CAS  PubMed  Google Scholar 

  3. Levick JR, Michel CC (2010) Microvascular fluid exchange and the revised Starling principle. Cardiovasc Res 87(2): 198–210. https://doi.org/10.1093/cvr/cvq062

    Article  CAS  PubMed  Google Scholar 

  4. Goswami AK, Khaja MS, Downing T, Kokabi N, Saad WE, Majdalany BS (2020) Lymphatic Anatomy and Physiology. Semin Intervent Radiol 37(3): 227–236. https://doi.org/10.1055/s-0040-1713440

    Article  PubMed  PubMed Central  Google Scholar 

  5. Macpherson AJ, Smith K (2006) Mesenteric lymph nodes at the center of immune anatomy. J Exp Med 203(3): 497–500. https://doi.org/10.1084/jem.20060227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. von der Weid PY (2019) Lymphatic Vessel Pumping. Adv Exp Med Biol 1124: 357–377. https://doi.org/10.1007/978-981-13-5895-1_15

    Article  CAS  PubMed  Google Scholar 

  7. Steele MM, Lund AW (2021) Afferent Lymphatic Transport and Peripheral Tissue Immunity. J Immunol 206(2): 264–272. https://doi.org/10.4049/jimmunol.2001060

    Article  CAS  PubMed  Google Scholar 

  8. Breslin JW, Yang Y, Scallan JP, Sweat RS, Adderley SP, Murfee WL (2018) Lymphatic Vessel Network Structure and Physiology. Compr Physiol 9(1): 207–299. https://doi.org/10.1002/cphy.c180015

    Article  PubMed  PubMed Central  Google Scholar 

  9. Solari E, Marcozzi C, Negrini D, Moriondo A (2020) Lymphatic Vessels and Their Surroundings: How Local Physical Factors Affect Lymph Flow. Biology (Basel) 9(12): 463. https://doi.org/10.3390/biology9120463

  10. Lobov GI, Orlov RS (1995) The cellular mechanisms in the regulation of lymph transport. Russ J Physiol 81(6): 19–28. (In Russ).

    CAS  Google Scholar 

  11. Zweifach BW, Prather JW (1975) Micromanipulation of pressure in terminal lymphatics in the mesentery. Am J Physiol 228(5): 1326–1335. https://doi.org/10.1152/ajplegacy.1975.228.5.1326

    Article  CAS  PubMed  Google Scholar 

  12. Scallan JP, Zawieja SD, Castorena-Gonzalez JA, Davis MJ (2016) Lymphatic pumping: mechanics, mechanisms and malfunction. J Physiol 594(20): 5749–5768. https://doi.org/10.1113/JP272088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Olszewski W, Engeset A, Jaeger PM, Sokolowski J, Theodorsen L (1977) Flow and composition of leg lymph in normal men during venous stasis, muscular activity and local hyperthermia. Acta Physiol Scand 99(2): 149–155. https://doi.org/10.1111/j.1748-1716.1977.tb10365.x

    Article  CAS  PubMed  Google Scholar 

  14. Lobov GI, Orlov RS (1988) Self-regulation of the pump function of the lymphangion. Fiziol Zh SSSR Im IM Sechenova. 74(7): 977–986. (In Russ).

    CAS  Google Scholar 

  15. Muthuchamy M, Zawieja D (2008) Molecular regulation of lymphatic contractility. Ann N Y Acad Sci 1131: 89–99. https://doi.org/10.1196/annals.1413.008

    Article  PubMed  Google Scholar 

  16. Willard-Mack CL (2006) Normal structure, function, and histology of lymph nodes. Toxicol Pathol 34(5): 409–424. https://doi.org/10.1080/01926230600867727

    Article  PubMed  Google Scholar 

  17. von Andrian UH, Mempel TR (2003) Homing and cellular traffic in lymph nodes. Nature Rev Immunol 3: 867–878. https://doi.org/10.1038/nri1222

    Article  CAS  Google Scholar 

  18. Ohtani O, Ohtani Y (2008) Structure and function of rat lymph nodes. Arch Histol Cytol 71(2): 69–76. https://doi.org/10.1679/aohc.71.69

    Article  PubMed  Google Scholar 

  19. Randolph GJ, Ivanov S, Zinselmeyer BH, Scallan JP (2017) The Lymphatic System: Integral Roles in Immunity. Annu Rev Immunol 35: 31–52. https://doi.org/10.1146/annurev-immunol-041015-055354

    Article  CAS  PubMed  Google Scholar 

  20. Hughes GA, Allen JM (1993) Neural modulation of bovine mesenteric lymph node contraction. Exp Physiol 78(5): 663–674. https://doi.org/10.1113/expphysiol.1993.sp003714

    Article  CAS  PubMed  Google Scholar 

  21. Lobov GI, Pan’kova MN (2012) Effect of histamine on contractile activity of smooth muscles in bovine mesenteric lymph nodes. Bull Exp Biol Med 152(4): 406–408. https://doi.org/10.1007/s10517-012-1539-5

    Article  CAS  PubMed  Google Scholar 

  22. Chi Y, Liang J, Yan D (2006) A material sensitivity study on the accuracy of deformable organ registration using linear biomechanical models. Med Phys 33(2): 421–433. https://doi.org/10.1118/1.2163838

    Article  CAS  PubMed  Google Scholar 

  23. Hope SA, Hughes AD (2007) Drug effects on the mechanical properties of large arteries in humans. Clin Exp Pharmacol Physiol 34(7): 688–693. https://doi.org/10.1111/j.1440-1681.2007.04661.x

    Article  CAS  PubMed  Google Scholar 

  24. Arkill KP, Moger J, Winlove CP (2010) The structure and mechanical properties of collecting lymphatic vessels: an investigation using multimodal nonlinear microscopy. J Anat 216(5): 547–555. https://doi.org/10.1111/j.1469-7580.2010.01215.x

    Article  PubMed  PubMed Central  Google Scholar 

  25. Ohhashi T, Azuma T, Sakaguchi M (1980) Active and passive mechanical characteristics of bovine mesenteric lymphatics. Am J Physiol 239(1): H88–H95. https://doi.org/10.1152/ajpheart.1980.239.1.H88

    Article  CAS  PubMed  Google Scholar 

  26. Ferguson MK, Williams U, Leff AR, Mitchell RW (1993) Length-tension characteristics of bovine tracheobronchial lymphatic smooth muscle. Lymphology 26: 19–24

    CAS  PubMed  Google Scholar 

  27. Razavi MS, Dixon JB, Gleason RL (2020) Characterization of rat tail lymphatic contractility and biomechanics: incorporating nitric oxide-mediated vasoregulation. J R Soc Interface 17(170): 20200598. https://doi.org/10.1098/rsif.2020.0598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Folse DS, Beathard GA, Granholm NA (1975) Smooth muscle in lymph node capsule and trabeculae. Anat Rec 183(4): 517–521.

    Article  CAS  PubMed  Google Scholar 

  29. Castenholz A (1990) Architecture of the lymph node with regard to its function. Curr Top Pathol 84 (Pt 1): 1–32. https://doi.org/10.1007/978-3-642-75519-4_1

    Article  PubMed  Google Scholar 

  30. Zhdanov DA (1970) Regional characteristics and age-related changes in the structure and cytoarchitectonics of human lymph nodes. Arkh Patol 32(3): 14–23.

    CAS  PubMed  Google Scholar 

  31. Hadamitzky C, Spohr H, Debertin AS, Guddat S, Tsokos M, Pabst R (2010) Age-dependent histoarchitectural changes in human lymph nodes: an underestimated process with clinical relevance? J Anat 216(5): 556–562. https://doi.org/10.1111/j.1469-7580.2010.01213.x

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sapin MR (1977) Anatomy of the connective tissue framework of adult human lymph nodes. Arkh Anat Gistol Embriol 72(4): 58–65. (In Russ).

    CAS  PubMed  Google Scholar 

  33. Geelhoed GW (1996) "Aging bull'. Med Hypotheses 47(6): 471–479. https://doi.org/10.1016/s0306-9877(96)90160-7

    Article  CAS  PubMed  Google Scholar 

  34. Zhang RZ, Gashev AA, Zawieja DC, Davis MJ (2007) Length-tension relationships of small arteries, veins, and lymphatics from the rat mesenteric microcirculation. Am J Physiol Heart Circ Physiol 292(4): H1943–H1952. https://doi.org/10.1152/ajpheart.01000.2005

    Article  CAS  PubMed  Google Scholar 

  35. Novkovic M, Onder L, Cheng HW, Bocharov G, Ludewig B (2018) Integrative Computational Modeling of the Lymph Node Stromal Cell Landscape. Front Immunol 23(9): 2428. https://doi.org/10.3389/fimmu.2018.02428

    Article  CAS  Google Scholar 

  36. Hsu MC, Itkin M (2016) Lymphatic Anatomy. Tech Vasc Interv Radiol 19(4): 247–254. https://doi.org/10.1053/j.tvir.2016.10.003

    Article  PubMed  Google Scholar 

  37. Bernier-Latmani J, Petrova TV (2017) Intestinal lymphatic vasculature: structure, mechanisms and functions. Nat Rev Gastroenterol Hepatol 14(9): 510–526. https://doi.org/10.1038/nrgastro.2017.79

    Article  CAS  PubMed  Google Scholar 

  38. Pabst O, Mowat AM (2012) Oral tolerance to food protein. Mucosal Immunol 5: 232–239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li L, Wu J, Abdi R, Jewell CM, Bromberg JS (2021) Lymph node fibroblastic reticular cells steer immune responses.Trends Immunol 42(8): 723–734. https://doi.org/10.1016/j.it.2021.06.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Faroon OM, Henry RW, al-Bagdadi FK (1987) Smooth muscle distribution in the capsule and trabeculae of the caprine superficial cervical lymph node. Histol Histopathol 2(3): 313–315.

    CAS  PubMed  Google Scholar 

  41. Pastukhova IA (1986) Myocytes of the inguinal lymph nodes. Arkh Anat Gistol Embriol 90(6): 32–37. (In Russ).

    CAS  PubMed  Google Scholar 

  42. Erofeeva LM, Mnikhovich MV (2020) Structural and Functional Changes in the Mesenteric Lymph Nodes in Humans during Aging. Bull Exp Biol Med 168(5): 694–698. https://doi.org/10.1007/s10517-020-04782-0

    Article  CAS  PubMed  Google Scholar 

  43. Ahmadi O, McCall JL, Stringer MD (2013) Does senescence affect lymph node number and morphology? A systematic review. ANZ J Surg 83(9): 612–618. https://doi.org/10.1111/ans.12067

    Article  PubMed  Google Scholar 

  44. Jamalian S, Bertram CD, Richardson WJ, Moore JE Jr (2013) Parameter sensitivity analysis of a lumped-parameter model of a chain of lymphangions in series. Am J Physiol Heart Circul Physiol 305(12): H1709–H1717. https://doi.org/10.1152/ajpheart.00403.2013

    Article  CAS  Google Scholar 

  45. Zhang R, Gashev AA, Zawieja DC, Lane MM, Davis MJ (2007) Length-dependence of lymphatic phasic contractile activity under isometric and isobaric conditions. Microcirculation 14(6): 613–625. https://doi.org/10.1080/1073968070143616

    Article  PubMed  Google Scholar 

  46. Telinius N, Drewsen N, Pilegaard H, Kold-Petersen H, de Leval M, Aalkjaer C, Hjortdal V, Boedtkjer DB (2010) Human thoracic duct in vitro: diameter-tension properties, spontaneous and evoked contractile activity. Am J Physiol Heart Circ Physiol 299(3): H811–H818. https://doi.org/10.1152/ajpheart.01089.2009

    Article  CAS  PubMed  Google Scholar 

  47. Shirasawa Y, Benoit JN (2003) Stretch-induced calcium sensitization of rat lymphatic smooth muscle. Am J Physiol Heart Circ Physiol 285: H2573–H2577.

    Article  CAS  PubMed  Google Scholar 

  48. Davis MJ, Davidson J (2002) Force–velocity relationship of myogenically active arterioles. Am J Physiol Heart Circ Physiol 282: H165–H174.

    Article  CAS  PubMed  Google Scholar 

  49. Browse NL, Doig RL, Sizeland D (1984) The resistance of a lymph node to lymph flow. Br J Surg 71(3): 192–196. https://doi.org/10.1002/bjs.1800710308

    Article  CAS  PubMed  Google Scholar 

  50. Borisov AV (2005) Functional anatomy of lymphangion. Morfologiia. 128(6): 18–27. (In Russ).

    CAS  PubMed  Google Scholar 

  51. Iosifov GM (1914) The human lymphatic system with a description of the adenoids and organs of lymphatic movement. Ed Tomsk Univer, Tomsk. (In Russ).

    Google Scholar 

  52. McHale NG, Roddie IC (1976) The effect of transmural pressure on pumping activity in isolated bovine lymphatic vessels. J Physiol 261(2): 255–269. https://doi.org/10.1113/jphysiol.1976.sp011557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ferguson MK, Williams U (2000) Measurement of flow characteristics during individual contractions in bovine mesenteric lymphatic vessels. Lymphology 33(2): 36–42.

    CAS  PubMed  Google Scholar 

  54. McGeown JG, McHale NG, Thornbury KD (1987) The effect of electrical stimulation of the sympathetic chain on peripheral lymph flow in the anaesthetized sheep. J Physiol 393: 123–133. https://doi.org/10.1113/jphysiol.1987.sp016814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. McGeown JG, McHale NG, Thornbury KD (1987) The role of external compression and movement in lymph propulsion in the sheep hind limb. J Physiol 387: 83–93. https://doi.org/10.1113/jphysiol.1987.sp016564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Scallan JP, Zawieja SD, Castorena-Gonzalez JA, Davis MJ (2016) Lymphatic pumping: mechanics, mechanisms and malfunction. J Physiol 594(20): 5749–5768. https://doi.org/10.1113/JP272088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Benoit JN, Zawieja DC, Goodman AH, Granger HJ (1989) Characterization of intact mesenteric lymphatic pump and its responsiveness to acute edemagenic stress. Am J Physiol 257(6 Pt 2): H2059–H2069. https://doi.org/10.1152/ajpheart.1989.257.6.H2059

    Article  CAS  PubMed  Google Scholar 

  58. Bouta EM, Wood RW, Brown EB, Rahimi H, Ritchlin CT, Schwarz EM (2014) In vivo quantification of lymph viscosity and pressure in lymphatic vessels and draining lymph nodes of arthritic joints in mice. J Physiol 592(6): 1213–1223. https://doi.org/10.1113/jphysiol.2013.266700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Nathanson SD, Mahan M (2011) Sentinel lymph node pressure in breast cancer. Ann Surg Oncol 18(13): 3791–3796. https://doi.org/10.1245/s10434-011-1796-y

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Russian Science Foundation (RSF), grant no. 22-25-00108.

Author information

Authors and Affiliations

  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    G. I. Lobov & M. E. Kosareva

Authors
  1. G. I. Lobov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. E. Kosareva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization and experimental design, data collection, editing the manuscript (G.I.L.); experimental work, writing the manuscript (M.E.K.).

Corresponding author

Correspondence to G. I. Lobov.

Ethics declarations

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest related to the publication of this article.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2022, Vol. 58, No. 5, pp. 423–435https://doi.org/10.31857/S0044452922050072.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lobov, G.I., Kosareva, M.E. Comparative Characterization of Capsule Mechanical Properties in Mesenteric Lymph Nodes of Young and Aging Bulls. J Evol Biochem Phys 58, 1353–1366 (2022). https://doi.org/10.1134/S0022093022050076

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0022093022050076

Keywords:

Search

Navigation