Developmental Biology Biology Fertilization. October 19, 2006

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1 Developmental Biology Biology 4361 Fertilization October 19, 2006

2 Fertilization Fertilization accomplishes two things: Sex (combining genes from two genomes) Reproduction (initiates reactions in the egg cytoplasm that allow development to proceed) Major Events: 1. Contact and recognition between sperm and eggs. species specificity 2. Regulation of sperm entry into egg. 3. Fusion of genetic material of sperm and egg. 4. Activation of egg metabolism to start development. Lennart Nilsson

3 Fertilization Overview Model species: sea urchin & human Sperm formation and structure Egg structure and function Interactions between sperm and eggs Chemoattraction Acrosome reaction Binding and fusion Prevention of polyspermy Egg activation

4 Sperm Formation

5 Sperm Axoneme

6 The Egg All material necessary for the beginning of development and growth must be stored in the egg. eggs actively accumulate material as they develop: proteins yolk (made in other organs (liver, fat bodies), transported to egg ribosomes and trna mrna burst of protein synthesis after fertilization encode proteins for use in early development morphogenic factors direct differentiation of cells into certain types transcription factors, paracrine factors some localized regionally; segregated into different cells during cleavage protective chemicals UV filters DNA repair enzymes antibodies alkaloids (and other protective molecules)

7 Egg Maturation at Sperm Entry Fertilization activates the egg; including release from meiotic arrest

8 Egg Maturation at Sperm Entry

9 Sea Urchin Egg Structure Volume: 2 x 10 4 mm 3 (200 picoliters) > 200 X sperm volume cell membrane fusion with sperm cell membrane regulates ion flow extracellular envelope inverts vitelline envelope fibrous mat sperm egg recognition contains glycoproteins ( vertebrates zona pellucida) egg jelly glycoprotein meshwork attract or activate sperm

10 Mammalian Egg cumulus ovarian follicular cells inner most layer corona radiata

11 Egg Membrane Structure egg jelly actin microvilli filamentous (f actin) cortex globular (g actin) cortex Cortical granules: Golgi derived ~15k/sea urchin egg proteolytic enzymes hyaline protein mucopolysaccharides adhesive glycoproteins

12 Interaction Between Egg and Sperm General steps: 1. Chemoattraction of sperm to egg soluble molecules released by egg 2. Exocytosis of the acrosome stimulated by binding of egg molecules 3. Binding of sperm to the extracellular envelope usually a multi step process involves binding molecules and receptors located on each gamete 4. Passage of sperm through the extracellular envelope 5. Fusion of the egg and sperm cell membranes sperm and egg pronuclei meet, fuse; development initiated

13 Sea Urchin Fertilization Challenges for sea urchins (and others): how to bring two very small cells together in a very large space how to ensure that only sperm and eggs of the same species join

14 Sperm Chemoattraction Arbacia punctulata resact A. 0 sec B. 20 sec 14 aa peptide source egg jelly species specific membrane resact receptors binding: guanylyl cyclase cgmp activates Ca 2+ channel Ca 2+ provides directional cue C. 40 sec D. 90 sec

15 Sperm Egg Interaction Sea Urchin

16 Acrosome Reaction Sea Urchin AR stimulated by contact with egg jelly species specific stimulatory molecules in S. purpuratus fucose sulfate fucose sulfate binding to sperm receptor activates: Ca 2+ transport channel allows Ca 2+ into sperm head Na + /H + exchanger pumps Na + in/h + out phospholipase produces inositol trisphosphate (IP 3 ) elevated Ca 2+ and basic cytoplasm triggers fusion of acrosomal and cell membranes proteolytic enzymes digest a path through jelly coat to surface

17 Acrosome Reaction Sea Urchin Ca 2+ influx stimulates g actin polymerization to f actin acrosomal process adheres to vitelline envelope through bindin protein bindin species specific binding to receptor on vitelline envelope

18 Vitelline Membrane Bindin Receptors regular distribution species specificity

19 Fusion of Sperm and Egg Membranes acrosomal process adheres to egg membrane microvilli membranes fuse (fusogenic protein?) causes egg actin polymerization fertilization cone formed actin from both gametes form connections sperm nucleus and tail pass through cytoplasmic bridge

20 Prevention of Polyspermy More than one sperm entry into egg results in polyploid situation; eventual death. Fast block to polyspermy electrical sea urchins, frogs, not in most mammals (why not??) Slow block to polyspermy chemical, physical most species, including mammals

21 Fast Block to Polyspermy cell membranes provide a selective ionic barrier: cytoplasm/extracellular seawater: high Na+, low K+ (relatively) cytoplasm low Na+, high K+ (relatively) ionic imbalance maintained by membrane pumps, exchangers ionic imbalance creates an electrical potential across the membrane; ~ 70 mv 1 3 sec after sperm binding, membrane potential shifts positively; ~ +20 mv sperm cannot bind to eggs with positive membrane potential NOTE transient

22 Slow Block to Polyspermy Cortical granule reaction chemical and mechanical block active ~ 1 min after sperm egg fusion Cortical granules contained just beneath plasma membrane ~ 15,000 granules/sea urchin egg ~ 1 μm diameter Sperm entry stimulates fusion of cortical granule membrane with cell membrane (like AR) CG contents released into the space between the cell membrane and vitelline envelope 1. serine protease dissolves protein post connections between envelope and membrane clips off bindin receptors & connected sperm 2. mucopolysaccharides sticky compounds; produce osmotic pressure water rushes in, envelope raises 3. peroxidases oxidizes, crosslinks tyrosines hardens fertilization envelope 4. hyaline (protein) forms a coating around the egg: hyaline layer

23 Cortical Granule Exocytosis 1 elevation of vitelline membrane cortical granule fusion; release of CG contents

24 Cortical Granule Exocytosis 2 hyaline layer

25 Fertilization Envelope Time after sperm addition: 10 sec 25 sec 35 sec

26 Ca 2+ Role in Cortical Granule Reaction Cortical granule reaction mechanism similar to acrosome reaction. at fertilization, egg cytoplasmic Ca 2+ concentration rises high Ca 2+ causes cortical granule membranes to fuse with cell membrane internal Ca 2+ released as a self propagating wave Ca 2+ causes advancing cortical granule exocytosis, fertilization envelope, etc. 1 2 t t 30 sec

27 Activation of Egg Metabolism Fertilization results in: 1. merging of two haploid nuclei 2. initiating the processes that start development these events happen in the cytoplasm occur without nuclear involvement Sperm fusion activates egg metabolism stimulates a preprogrammed set of metabolic events into action early responses occur within seconds of cortical reaction late responses start within minutes after fertilization

28 Egg Activation Pathway Early Responses

29 Egg Activation Pathway Late Responses

30 Early Responses Ca 2+ release at fertilization increases concentration from μm Ca 2+ activates metabolic reactions NAD + kinase burst of O 2 reduction (to H 2 O 2 )

31 Late Responses

32 sperm nuclear envelope vesiculates sperm DNA decondenses transcription and replication can start Pronuclear Fusion in sea urchins, fertilization occurs after 2 nd meiotic division therefore, a haploid female pronucleus is already present at fertilization after cell membrane fusion, sperm nucleus and centriole separate from mitochondria and flagellum sperm flagellum and mitochondria disintegrate sperm pronucleus rotates 180 so that sperm centriole is between the sperm and egg pronuclei sperm centriole acts as a microtubule organizing center forms an aster microtubules extend throughout the egg; contact female pronucleus pronuclei migrate towards one another fusion forms diploid zygotic nucleus

33 Pronuclear Fusion

34 Mammalian Fertilization Sea urchin v. mammalian fertilization: many similarities, some differences: internal fertilization heterogeneity of sperm population translocation of gametes to the oviduct (transport and motility) sperm capacitation chemotaxis, thermotaxis, hyperactivation of motility recognition at the zona pellucida gamete adhesion sperm egg binding acrosome reaction prevention of polyspermy fusion of genetic material

35 Sperm Translocation and Capacitation The ovulated egg (surrounded by cumulus cells) picked up by the oviduct fimbriae ciliary beating and muscle contractions move oocyte cumulus complex into oviduct Sperm are ejaculated at the cervix, fertilize the egg at the ampulla of the fallopian tube motility not sufficient to move sperm to the ampulla sperm transported by the female reproductive tract uterine muscle contractions move sperm to the oviduct sperm transport slows at ampulla (sperm time release?) sperm motility important within the oviduct hyperactivated motility in the vicinity of the oocyte or cumulus directional cues from temperature gradients (thermotaxis)

36 Sperm Capacitation Capacitation a series of physiological maturation events that takes place in the vaginal tract, uterus, and oviduct Freshly ejaculated mammalian sperm cannot fertilize the egg non capacitated sperm are held up in the cumulus matrix capacitation requirements vary by species capacitation can be accomplished in vitro culture medium oviduct fluid albumin capacitation involves membrane lipid carbohydrate, and protein changes, membrane potential changes ( ), protein phosphorylation, internal ph changes, enzyme activation capacitation is a transient event; sperm become uncapacitated after a period WHY? Timing: nearly all human pregnancies result from sexual intercourse during a 6 day period ending on the day of ovulation. fertilizing sperm may take a long as 6 days to reach the ampulla

37 Hyperactivation, Thermotaxis, Chemotaxis Hyperactivation Sperm of some species change motility patterns in the oviduct hyperactivated motility higher velocity, greater force suited for viscous oviduct fluid Thermotaxis Sperm may be able to sense a thermal gradient ampulla of oviduct is 2 C warmer than isthmus only capacitated sperm can respond thermotactically Chemotaxis Oocytes and cumulus cells may secrete chemotactic agents follicular fluid shows some chemotactic ability only fertilizable follicles had chemotactic activity only capacitated sperm respond

38 Recognition at the Zona Pellucida Mammalian Zona Pellucida analogous to vitelline membrane sperm binding relatively species specific ZP (mouse): 3 glycoproteins ZP1, ZP2, ZP3 also, internal accessory proteins ZP matrix is synthesized by oocyte Sequential interactions between sperm proteins and zona components 1. Weak binding between sperm and peripheral egg protein 2. Stronger binding between zona and sperm SED1 protein 3. Sperm protein binds strongly to ZP3 ZP3 stimulates acrosome reaction

39 Mouse Sperm Acrosome Reaction Acrosome reaction induced when ZP3 crosslinks receptors on the sperm surface. sperm that undergo AR before reaching the zona are unable to penetrate AR induced when ZP3 crosslinks receptors on the sperm membrane sperm galactosyltransferase binds to N acetylglucosamine of ZP3 crosslinking activates specific G proteins in sperm membrane this initiates a cascade that opens membrane Ca 2+ channels Ca 2+ mediated exocytosis of the acrosomal vesicle

40 Gamete Fusion and Prevention of Polyspermy Mammalian sperm enter egg tangentially contact takes place on the side of the sperm membrane fusion at the junction of the inner acrosomal and cell membrane: equatorial region sperm binds to regions of the egg where actin polymerizes to extend microvilli to sperm Cortical granules release enzymes that modify ZP so that it can no longer bind sperm N acetylglucosiminidase cleaves part of ZP3 carbohydrate chain ZP2 is also clipped; loses ability to bind sperm

41 Essentially the same as sea urchin. Pronuclei Fusion mammalian pronuclear migration takes far longer (12 h v. ~ 1 h) glutathione from egg cytoplasm reduces disulfide bonds in protamines (replace histones in sperm nucleus) allows uncoiling of sperm chromatin replication and transcription allowed Mammalian oocyte nucleus is arrested in metaphase of 2 nd meiotic division when sperm enters Ca 2+ oscillations are initiated by sperm entry Ca 2+ inactivates MAP kinase allows DNA sythesis Ca 2+ also leads to proteolysis of cyclin allows cell cycle to continue

42 Fusion, cont. DNA synthesis occurs separately in male and female pronuclei male and female pronuclear chromatin condenses into chromosomes that orient themselves on a common mitotic spindle a true diploid nucleus in mammals is not seen in the zygote, but at the two cell stage (NOTE sea urchins produce a common zygote nucleus) Sperm contribute nucleus, mitochondria, centriole, small amount of cytoplasm mitochondria and mitochondrial DNA are degraded therefore, all mitochondria are derived from the mother several sperm proteins and mrnas for transcription and paracrine factors brought into the egg also, micrornas that may down regulate receptors involved in early cell division

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